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.     

Lactating Females Do Not Discriminate Between Their Own Young and Unrelated Pups in the Communally Breeding Rodent, Octodon degus

Females in numerous rodent species engage in communal nesting and breeding, in which they share one or more nests to rear their young. A potential cost of communal nesting and breeding is that mothers divert resources to unrelated offspring. One way mothers could avoid this cost is to recognize and favour their own young over unrelated offspring when allocating maternal effort. We assessed whether female degus (Octodon degus), a communally nesting and breeding caviomorph rodent, discriminate between their own and unrelated offspring during lactation. Female degus previously have been shown to distinguish between their own and unrelated pups when exposed to odours from both. We measured pup discrimination based on differences in the retrieval behaviour of females that were in early or intermediate lactation directed towards their own and unrelated offspring; offspring presented were of similar or different age. Before any event of pup retrieval, lactating females spent similar amounts of time and interacted to a similar extent with their own and unrelated pups. During pup retrieval, all lactating females transported both pups to the nest. Neither relatedness to pups, nor pup‐age differences, influenced the order in which pups were retrieved to the nest. Dams waited similar amounts of time before retrieving the first pup when the first transported young was their own or unrelated. Likewise, females waited similar amounts of time before retrieving the second pup when the pup transported first was their own or unrelated. The time between first and second pup transport events was longer when dams were in early when compared with intermediate lactation, but only when pups were of similar age. All experimental subjects nursed unrelated pups after they were retrieved. Collectively, our results do not support the hypothesis that communally breeding female degus use their recognition ability to discriminate against unrelated offspring in favour of their own young.     

Physical, hormonal and behavioural aspects of sexual development in the marmoset monkey, Callithrix jacchus.

Measurements of growth, plasma progesterone and testosterone levels, and copulatory behaviour were obtained from captive marmosets from birth until 600-800 days of age. Body weight and knee-to-heel length were similar for both sexes. Males exhibited a neonatal testosterone surge from 15-100 days and testosterone levels began to rise again, coincident with the growth of the testis, at about 250 days. The males were copulating by 400-500 days of age. Paired females were apparently ovulating and able to conceive from about 400 days. In peer groups, only the dominant female became pregnant, because subordinate females failed to ovulate.     

Significance of the weaning period for natality and maternal behaviour of laboratory rats.

Normally weaned females (at 30 days) displayed seasonal cyclic changes in natality and the characteristics of the young. Natality in the spring and summer was high, the litters were large, the proportion of females and males in the litter was equal and deaths among the unweaned young were very few. Natality in the autumn and winter was low and the litters were small and consisted mainly of males. The death rate among the young was higher than in the spring and summer. Prematurely weaned females (at 15 days) displayed no seasonal cycle either in natality or in the characteristics of the young. The studied parameters corresponded to the values found in the spring and summer in normally weaned females. No differences were found in maternal retrieving, but there was a marked difference in nest-building. The normally weaned female tore up paper (building material) into small fragments 24 hours before giving birth and dropped the young into a soft nest of finely shredded paper. On leaving the nest it covered the young up. The prematurely weaned female scattered the paper about the cage 24 hours before giving birth and dropped the young into a depression stamped out among whole pieces of paper. It did not cover the young up on leaving the nest. The cause of the difference in building behaviour is evidently that prematurely weaned females failed to acquire early experience of this behaviour between the 15th and 30th day of life.     

Factor affecting body mass of young fat dormics (Glis glis) at weaning and by hibernation

This paper describes the factors affecting body mass at weaning and by hibernation of young fat dormice (Glis glis) We studied a free-living population in 1991 and 1992 in a mixed forest where 100 nest-boxes were placed. In the two years, 128 females used the nest-boxes to give birth and rear their litters and more than 900 dormice have been individually marked. Body mass of young at weaning was positively correlated to body mass of the mother in both years and to birth date in 1991, while litter size was negatively correlated to body mass of the young in 1992 only, when birth took place about two weeks later than in 1991. On the contrary, by the time of hibernation, young born later weighed significantly less than those born earlier in the season, and heavier young at weaning remained heavier by hibernation, while maternal body mass and litter size did not significantly affect body mass of young at this stage. Body mass of the mother was negatively related to the date of parturition and early breeding females lost weight during lactation, while females that bred later did not. It seems, therefore, that early breeding carries a cost that only females in good condition can afford. It appears that females may follow two strategies: those in poor body condition will delay pregnancy so that lactation occurs when environmental feeding conditions are at their best; those in good condition will breed earlier, since they can afford to lose weight during lactation. Their young will have more time to grow before hibernation and the mothers themselves will have a longer period of time for restoring their fat reserves.     

Maternal behaviour of undernourished mother rats

Undernourished mother rats were given daily meals throughout most or all of pregnancy and lactation, comprising about half the amount of a good quality diet taken by controls. Their daily pattern of nest occupation and desertion during lactation was quite different from that of controls. Retrieving tests were carried out at 4, 6, 8 and 10 days after parturition. Underfed mothers were less efficient than controls in retrieving their young on days 8 and 10, and were less likely to lick their young during the test period. They also spent much more time rearing on their hind legs. Among undernourished females the number of young retrieved was negatively correlated with duration of rearing. The significance of the differences in maternal behaviour for offspring development is discussed.     

Age affects the expression of maternal care and subsequent behavioural development of offspring in a precocial bird

Variations of breeding success with age have been studied largely in iteroparous species and particularly in birds: survival of offspring increases with parental age until senescence. Nevertheless, these results are from observations of free-living individuals and therefore, it remains impossible to determine whether these variations result from parental investment or efficiency or both, and whether these variations occur during the prenatal or the postnatal stage or during both. Our study aimed first, to determine whether age had an impact on the expression of maternal breeding care by comparing inexperienced female birds of two different ages, and second, to define how these potential differences impact chicks' growth and behavioural development. We made 22 2-month-old and 22 8-month-old female Japanese quail foster 1-day-old chicks. We observed their maternal behaviour until the chicks were 11 days old and then tested these chicks after separation from their mothers. Several behavioural tests estimated their fearfulness and their sociality. We observed first that a longer induction was required for young females to express maternal behaviour. Subsequently as many young females as elder females expressed maternal behaviour, but young females warmed chicks less, expressed less covering postures and rejected their chicks more. Chicks brooded by elder females presented higher growth rates and more fearfulness and sociality. Our results reveal that maternal investment increased with age independently of maternal experience, suggesting modification of hormone levels implied in maternal behaviour. Isolated effects of maternal experience should now be assessed in females of the same age. In addition, our results show, for first time in birds, that variations in maternal care directly induce important differences in the behavioural development of chicks. Finally, our results confirm that Japanese quail remains a great laboratory model of avian maternal behaviour and that the way we sample maternal behaviour is highly productive.     

Effect of food restriction on reproduction and lactation in house mice mated post partum

Primiparous, post-partum mated BALB/c bom inbred mice were allowed to raise litters of 6 young until Day 22 of lactation: 11 of 25 females were restricted to 60% of food consumption of ad-libitum fed dams after stud male removal at Day 2 of lactation. Since weight gain of restricted females during lactation was not inhibited and infanticidal behaviour was not enhanced, food deprivation can be considered to have been relatively mild. However, none of the food-restricted dams gave birth to a second litter whereas 12 of the 14 ad-libitum fed mice littered. This pregnancy failure is suggested to be due to implantation failure or abortion shortly after implantation, which is attributed to maternal manipulation rather than to immediate consequences of energetic demands of lactated young. The dynamics of the weight changes of dams and young suggest that milk production in suckling house mice drops most markedly between Days 17 and 18 of lactation, irrespective of whether the dams are non-pregnant, pregnant, or food-restricted.     

Sexual and maternal behaviour at the postpartum oestrus: The role of experience in time-sharing

The postpartum sexual and maternal behaviour of Norway rats (Rattus norvegicus) was observed in a seminatural habitat. Behavioural decision-making by the female was examined by disrupting the nest and newborn offspring during mating. In experiment 1, multiparous females responded to nest disruption with an increase in maternal behaviour that was largely restricted to the post-ejaculatory intervals. The temporal and frequency measures of copulation were largely unaffected, implicating behavioural time-sharing. In experiment 2, following nest disruption primiparous females did not switch efficiently between maternal and sexual behaviour, showed poor retrieval of pups, and returned to the nest during ejaculatory series. They did not display the characteristics of behavioural time-sharing, indicating that previous experience may play a role in the ability to time-share.     

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.     

Rank Acquisition Through Birth Order in Mouflon Sheep (Ovis gmelini) Ewes

The relationship between mothers' and daughters' dominance ranks was studied in a captive herd of mouflon sheep ( Ovis gmelini ), including nine adult ewes and their daughters, observed as lambs and yearlings. We found a positive correlation between the ranks of mothers and those of their yearling daughters, even though every mother dominated all the yearlings. We then tested the hypothesis that daughters from subordinate ewes became subordinate within their own age class because, as lambs, they had received more aggression from the other ewes in the herd. Recorded data were inconsistent with the hypothesis, even showing a trend for female lambs to receive aggression more frequently when born from dominant ewes. We also tested the hypothesis that resemblance between mothers' and daughters' ranks was due to inheritance of aggressiveness. No significant correlation was found between mothers' and daughters' aggressiveness, so the hypothesis was not supported. Finally, we found a significant concordance between mothers' ranks, daughters' ranks, and daughters' birth dates. Earlier-born daughters became dominant over later-born ones, probably because of larger body size and more advanced social behaviour. The age of most of the mothers was undetermined, but in mouflon sheep, older ewes generally dominate younger ewes and are known to lamb earlier during the birth season. Accordingly, it is suggested that dominant ewes have daughters dominant in their own age class, because (1) age influences the parturition date during the birth season, and (2) age strongly influences rank, even in individuals born during the same lambing season.     

Reproductive suppression in female Alpine marmots, Marmota marmota

We studied mechanisms responsible for reproductive skew in female Alpine marmots. In each social group, only dominant females produced weaned young although subordinate females had similar body condition, were fertile as indicated by high levels of oestradiol during the mating season, and occasionally started pregnancies. During the period of gestation, dominant females initiated significantly more agonistic interactions against subordinate females, resulting in significantly increased levels of glucocorticoids and decreased levels of progesterone in subordinates. Results suggested that reproductive suppression in female Alpine marmots is mediated by the negative effects of stress (glucocorticoids) on the activity of the hypothalamic-pituitary-gonadal axis. The strength of competition between subordinate and dominant females was affected by their relatedness. Dominant females attacked unrelated subordinate females more, whereas amicable behaviour was observed mainly between dominant females and their daughters. These differences could be explained by differences in indirect fitness: related subordinate females benefited from warming the offspring of the dominant female during hibernation. Reproductive suppression was apparently costly for dominant females, because their reproductive success decreased as the number of adult subordinate females in a group increased. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Reproductive life history correlates of early and late sexual maturation in female Mongolian gerbils (Meriones unguiculatus)

Age at vaginal introitus is bimodally distributed in female domesticated Mongolian gerbils; some exhibit vaginal perforation before eye-opening (day 16), others after weaning (day 25). We found early- and late-maturing female gerbils to differ significantly in reproductive life history. Early-maturing females first reproduced when younger, had more litters, with more young per litter, and consequently had more than twice as many offspring as late-maturing females. In comparison with late-maturing females, early-maturing females gave birth to and weaned a greater proportion of females per litter and a higher proportion of early-maturing daughters per litter. Further, early-maturing females exhibited reduced maternal behaviour; they spent less time nursing their young and retrieved fewer offspring displaced from the nest than late-maturing females. Even under constant laboratory conditions, there were significant, correlated, circannual rhythms in female fecundity, the proportion of males per litter and the proportion of early-maturing daughters per litter. Review of the field literature suggests that wild Mongolian gerbils may exhibit similar variability in reproductive pattern.     

High rates of pregnancy loss by subordinates leads to high reproductive skew in wild golden lion tamarins (Leontopithecus rosalia)

Across taxa, cooperative breeding has been associated with high reproductive skew. Cooperatively breeding golden lion tamarins (Leontopithecus rosalia) were long thought to have a monogynous mating system in which reproduction was limited to a single dominant female. Subordinates with few reproductive opportunities delayed dispersal and remained in the natal group to provide alloparental care to siblings, thus allowing dominant reproductive females to meet the energetic needs associated with high rates of reproduction and successful infant rearing. The goal of this study was to re-assess monogyny in wild golden lion tamarin groups based upon pregnancy diagnoses that used non-invasive enzyme immunoassay for progesterone and cortisol, combined with weekly data on individual weight gain, bi-annual physical examinations noting pregnancy and lactation status and daily behavioral observations. We established quantitative and qualitative criteria to detect and determine the timing of pregnancies that did not result in the birth of infants. Pregnancy polygyny occurred in 83% of golden lion tamarin groups studied. The loss of 64% of subordinate pregnancies compared to only 15% by dominant females limited reproductive success mainly to dominant females, thus maintaining high reproductive skew in female golden lion tamarins. Pregnancy loss by subordinate adults did not appear to result from dominant interference in subordinate hormonal mechanisms, but more likely resulted from subordinate abandonment of newborn infants to mitigate dominant aggression.     

Male dominance status,female choice and mating success in the brown lemming, Lemmus trimucronatus

The objective of this study was to determine whether female brown lemmings would selectively mate with dominant conspecific males. In dyadic encounters, oestrous females paired with dominant males engaged in more frequent lordosis and contact social behaviours than those paired with subordinate males. However, the mount and thrust scores of dominant and subordinate males did not differ significantly. When females had simultaneous access to tethered dominant and subordinate males, they spent more time in close proximity to dominant males and avoided contact with subordinate males. Copulation scores were higher with dominant males. In triadic encounters with free-moving dominant and subordinate males, oestrous females spent more time near, and engaged in more sexual behaviour with, dominant males. Intermale agonistic interactions resulted in ‘privileged access’ to females by dominant males. Sexual behaviour scores were lower and there was a 10-fold increase in intermale aggression in triadic encounters between females and unfamiliar dominant and subordinate males. Both intermale agonistic interactions and female ‘choice’ behaviour accounted for the differential copulatory success of dominant males.     

Reproductive performance in grey seals: age-related improvement and senescence in a capital breeder

1. Three hypotheses have been advanced to account for age-related improvement in performance: the selection hypothesis predicts improved due to the loss of lower quality phenotypes, the constraint hypothesis predicts individuals improve function, and the restraint hypothesis predicts younger individuals forego or reduce effort because of mortality risks. A decline in age-related performance (i.e. senescence) is predicted by mutation accumulation, antagonistic pleiotropy and disposable soma (wear and tear) hypotheses. 2. Using five measures of performance - birth rate, maternal and pup birth mass, pup weaning mass, weaning success and lactation length - we tested these hypotheses concerning age-related change in reproduction in 279 female grey seals (Halichoerus grypus), ages 4-42 years, over a 23-year period between 1983 and 2005 on Sable Island, Nova Scotia. These females produced 2071 pups. 3. Although body mass of primiparous females increased with age (4-7 years) birth mass of their pups did not, but pup weaning mass did. Second- and third-parity females of the same age as primiparous females gave birth to and weaned heavier pups. However, parity and age were dropped from models when maternal body mass was included. 4. The proportion of females giving birth varied significantly with maternal age, increasing in young females and then declining late in life. Weaning success rate also increased rapidly to about 8 years and subsequently declined in females > 32 years. 5. Generalized additive models indicated nonlinear changes in 3 day body mass (i.e. approximately birth mass) and weaning mass of pups as a function of maternal age, after accounting statistically for the effects of maternal body mass. Mixed-effects, repeated-measures models fitted to longitudinal data further supported the conclusion that pup birth mass and weaning mass vary nonlinearly with maternal age and indicated nonlinear changes in lactation duration. 6. We found some support for the constraint hypothesis, but our findings were not consistent with the selection hypothesis or the restraint hypothesis as the basis for improvement in reproductive performance. 7. Senescence was evident in multiple female and offspring traits, indicating the degeneration in function of several physiological systems as predicted by the disposable soma hypothesis.     

A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum)

The maternal behaviour of three species of voles was compared using a semi-naturalistic laboratory system. Meadow vole females spent more time out of the nest, and exhibited less maternal behaviour in terms of nursing and brooding, and more non-social behaviour such as locomoting, eating, and drinking, than the females of the other two species. Across all species, maternal behaviour decreased from parturition onward, while non-social behaviour increased. Paternal care was well developed in the prairie vole and pine vole, but was never observed in the meadow vole. During the first postnatal week, male prairie voles showed a tendency to enter the nest when the female left the young unattended. This trend was not apparent in the male pine vole. The physical parameters of pup development, including eye opening and the development of fur, were similar in all three species. Behavioural development, however, was most rapid in the meadow vole, intermediate in the prairie vole, and slowest in the pine vole. These results are compared with those of previous field and laboratory studies, and are discussed with reference to the life-history strategy of each species.     

Observations on the maternal behaviour of free-ranging domestic pigs

The maternal behaviour of four gilts and one sow having her second litter was studied in two enclosures, measuring 7 and 13 ha. The females left the flocks approximately 24 h before farrowing and moved between 2.5 and 6.5 km during a period of continuous wandering lasting 4–6 h. During this wandering, the pigs seemed to examine and discriminate between different possible farrowing sites. When a site had been chosen, the pigs constructed nests resembling those reported for the European wild boar. After farrowing, the mother and litter remained in or close to the nest for about 9 days. Thereafter, the nests were suddenly abandoned and the piglets changed from hiders to followers. The female and the young joined the flock, but the litter tended to remain an intact social unit throughout lactation and mixed with other piglets only occassionally during resting. No cross-suckling was observed, although some attempts to steal milk from alien mothers were recorded. The piglets were weaned at between 14 and 17 weeks of age. The maternal behaviour was similar to that reported for wild boars and feral pigs. There were individual differences in maternal behaviour among the animals studied, which may be interpreted either as genetically fixed inter-individual differences or as variable strategies, adopted to increase the lifetime reproductive success.     

Energetics during reproduction: a doubly labeled water study of lactating baboons

Understanding the costs and regulation of reproduction in primates requires understanding the separate but linked effects of energy availability and total energy expenditure (TEE). We compared variation in TEE and energy intake (EI) between two periods, early lactation and after the resumption of sexual cycling, for eight females from two groups of normally reproducing colony-living baboons (Papio h. anubis). Total energy expenditure was assessed using the doubly labeled water method. TEE was correlated with maternal mass both during early lactation and after the resumption of cycling. TEE after the resumption of cycling was positively related to infant growth rates; mothers with rapidly growing infants had higher energy expenditure. TEE was however unrelated to maternal rank and only weakly associated with reproductive parameters such as delay to conception. EI in early lactation was related to infant mass and interbirth intervals, but unrelated to infant growth or reproductive parameters once cycling had resumed. Energy availability (EA; the difference between intake and expenditure) differed significantly between subordinate and dominant females during early lactation, was highly variable among individuals as a function of body composition, and is suggested to follow a nonlinear relationship as a complex function of social status, lactation stage, infant growth, and female fertility. Thus, as a consequence of reduced energy availability, subordinate females in this captive context may experience reproductive delays even though the total energy expenditure after the return of cycling was similar between high and low ranking females.