Litter reductions reveal a trade-off between offspring size and number in brown bears

Experimental manipulations have revealed positive effects of litter reduction on offspring mass in small mammals, but little is known about this trade-off in large mammals. We examined the determinants of natural litter size variation and quantified the effects of litter size, maternal characteristics, and litter composition on yearling mass using 24?years of data on marked brown bears (Ursus arctos) in Sweden. Infanticide by adult males is a major cause of cub-of-the-year mortality, leading to litter size reductions. Litter size (n?=?265) at den emergence ranged from one to four cubs (average, 2.7) and increased with maternal age. Litter size, however, appeared independent of maternal size, population density, interlitter interval, study area, or previous litter sex ratio. Yearling body mass increased with maternal body size but was independent of litter sex ratio. Litter size and yearling mass were negatively correlated, mostly because singletons were about 30?% heavier than yearlings from litters of two to four cubs. In reduced litters, survivors were on average 8?% heavier as yearlings than individuals from intact litters, suggesting that sibling competition reduces growth. Trade-offs between litter size and yearling mass in bears appear similar in magnitude to those found in small mammals.     

Maternal effects on post-weaning physical and social development in juvenile mountain goats (Oreamnos americanus)

Little is known about maternal effects on post-weaning development, yet they may be important because maternal care could have long-term consequences only evident when offspring approach adulthood. We have assessed the effects of maternal age, current reproduction (presence of a kid of the year) and social rank on the body mass, horn length and social rank of 1- and 2-year-old mountain goats (Oreamnos americanus). Maternal reproductive status and social rank did not affect the mass or horn length of either yearlings or 2-year-olds. Maternal age was positively correlated with yearling body mass for males but not females. We could not detect any maternal age effects on body mass of 2-year-olds. Maternal age and spring forage quality were positively correlated with horn length of yearlings of both sexes, but not of 2-year-olds. Juvenile females showed compensatory growth in mass between 1 and 2 years of age, but males did not. Neither sex showed compensatory growth in horn length. None of the maternal characteristics we examined directly affected the social rank of juveniles, which increased with body mass. Social rank in female mountain goats seems to be established early in life and maintained to adulthood. By affecting yearling development, maternal age could affect the reproductive success of males.     

Variation in litter size: a test of hypotheses in Richardson's ground squirrels

We studied litter size variation in a population of Richardson's ground squirrels (Spermophilus richardsonii) in Alberta, Canada, from 1987 to 2004. Litter size at first emergence of juveniles from the natal burrow ranged from 1 to 14; the most common litter sizes, collectively accounting for 41.0% of 999 litters, were 6 and 7. The number of offspring surviving to adulthood (attained on emergence from hibernation as yearlings) increased with increasing litter size, a result that was not predicted by Lack's "optimal litter size" hypothesis, Mountford's "cliff-edge" effect, or the "bad-years" effect. Contrary to the negative effects predicted by the "cost of reproduction" hypothesis, litter size had no significant influence on survival of mothers to the subsequent year or on the size of the subsequent litter. Rather, our results best fit the predictions of the "individual optimization" hypothesis, which suggests that litter size is determined by the body condition and environmental circumstances of each mother. Supporting this hypothesis, survival of individual offspring was not significantly associated with litter size. Additionally, year-to-year changes in maternal body mass at mating were positively associated with concurrent changes in litter size (r = 0.56), suggesting that litter size depends on the body condition of the mother. Because the mean number of recruits to adulthood increased as litter size increased (r2 = 0.96) and litter size increased with maternal condition, offspring productivity was greater for mothers in better body condition.     

Costs and benefits of communal rearing to female prairie voles (<Emphasis Type="Italic">Microtus ochrogaster</Emphasis>)

Communal rearing of offspring may help mothers maximize their investment in offspring at a reduced cost to their own bodily condition, thus maximizing their potential for reproductive success. The objective of this study was to quantify the costs and benefits of communal rearing to prairie vole (Microtus ochrogaster) pups and mothers. Mothers were assigned to one of three social units: solitary mothers, singularly breeding groups (i.e. one mother and one non-reproductive sister) and plurally breeding groups (i.e. two lactating sisters). For each type of social unit, some replicates were provided with food ad libitum, while others were provided with limited food. The body mass of focal mothers (i.e. the first mother to produce a litter) was a significant predictor of pup growth. Regardless of food availability, litters of focal mothers in plurally breeding groups gained more weight than litters reared by solitary mothers. Pups reared in singularly breeding groups were intermediate in weight gain, but did not gain significantly more weight than solitary offspring. There was no difference in the body mass of focal mothers from each type of social unit, regardless of food availability. Within plurally breeding groups, the weight gain of the two litters and body mass of focal and second mothers did not differ. However, focal mothers from plurally breeding groups nursed fewer pups than solitary mothers and also fewer pups than their nestmates when food was limited. Our results suggest that plural breeding results in greater fitness to mothers than solitary and singular breeding.Communicated by E. Korpimäki     

Weaning in the guinea pig (<Emphasis Type="Italic">Cavia aperea</Emphasis> f. <Emphasis Type="Italic">porcellus</Emphasis>): Who decides and by what measure?

Offspring should be selected to influence maternal effort to maximize their own fitness, whereas mothers are selected to limit investment in present progeny. In mammals, this leads to a conflict over the amount of milk provided and the timing of weaning. The intensity and time course of such conflict has so far mostly been investigated experimentally in altricial rodents. However, it is expected that offspring options for conflict will depend on developmental state. We therefore investigated in the highly precocial domestic guinea pig (Cavia aperea f. porcellus) who decides over nursing performance and weaning and how pup state influences these decisions. Specifically, we tested whether a threshold mass of pups predicts weaning time. By exchanging older litters against neonates and vice versa, we produced a situation in which females differed in lactational stage from the cross-fostered pups. Our results indicate that females decide about the timing of weaning, as cross-fostered younger pups were weaned at a much younger age than controls and older pups benefited from continuing lactation of foster mothers. Growth rates did not differ in the treatment groups, and different weaning ages resulted in differing weaning mass refuting the hypothesis that weaning is based on a threshold mass of offspring. This constitutes clear evidence that in a precocial rodent, the guinea pig, decisions about maternal care are primarily determined by maternal state and little influenced by pup state despite the extreme precociality of offspring. We suggest that precocial pups show little resistance to early weaning when food is abundant, as they reach sufficient nutritional independence by the middle of lactation to enable independent survival.     

Mixed sex allocation strategies in a polytocous mammal,the house mouse (<Emphasis Type="Italic">Mus musculus</Emphasis>)

The issue of adaptive adjustment of offspring sex ratio (proportion of male births) in polytocous mammals, producing several offspring per litter, is controversial because females of these species can maximize their fitness mainly by adjusting offspring number. To address this issue, we examined the effect of maternal condition at mating, experimentally decreased by pre-mating food restriction, on the sex ratio variation in 137 female mice. We tested two basic sex allocation hypotheses plausible for polytocous mammals: (1) the Myers hypothesis, predicting that cheaper sex should be favored in poor environmental conditions to maximize offspring number; and (2) the Williams hypothesis, predicting maximum fitness returns by adjusting size- and sex-specific composition of the litter according to the maternal condition. The food-restricted mothers produced larger litters with a higher proportion of cheaper daughters than the control mothers. By contrast, the control mothers optimized size and sex composition of the litter according to their weight at mating. In addition, the offspring of the food-restricted mothers suffered less from pre-weaning mortality than those of the control mothers. Therefore, when comparing the groups, the Myers hypothesis had a general significance while the Williams hypothesis was plausible only for the control mothers. Furthermore, some of the food-restricted mothers partly coped with the pre-mating food restriction and increased the proportion of sons in the litter with the increasing maternal weight loss (during the period of food restriction). The sex ratio variation was thus a result of three sex allocation strategies depending on the maternal condition at mating.     

Sex-specific preweaning maternal care in reindeer<Emphasis Type="Italic"> (Rangifer tarandus t.)</Emphasis>

Caribou (Rangifer tarandus) have been used as an example of a polygynous species in which one could expect females to manipulate their investments in sons and daughters based on their physical condition. We investigated whether the effect of maternal condition, measured as female body mass, on preweaning maternal care measured as calf mass in mid-July, calf mass in mid-November and calf mass gain (growth between mid-July and mid-November), was sex-biased in reindeer. We analysed separately young (h 4 years), prime age (5-10 years) and old (>10 years) mothers. Consistently, preweaning maternal care increased with increasing mother quality, but maternal condition did not influence whether a female produced a son or a daughter. Moreover, regardless of whether a female was young, prime age or old, there was no conclusive evidence of female quality-related, sex-biased preweaning maternal care in the study population. Our results indicate that maternal expenditure may be of equal magnitude in male and female offspring, regardless of the mothers' physical condition, and may support the hypothesis that a high level of maternal expenditure limits sex-biased maternal care.     

Age-related foetal sex ratio bias in Iberian red deer (<Emphasis Type="Italic">Cervus elaphus hispanicus</Emphasis>): are male calves too expensive for growing mothers?

Several theories predict offspring biases towards males or females with increasing reproductive resources of the mother to maximize reproductive returns by offspring, or as a result of prohibitive cost of the most expensive sex for young mothers or those in poor condition. This study examines foetus sex of 221 harvested hinds in a food-supplemented game estate for 10 years, according to hind age class (yearlings, subadults or adults), precise age, body mass and condition, and jaw length. A logistic model showed that hinds had a greater probability of bearing a male foetus with increasing age class, but not with any other variable. The greatest bias was found in yearling hinds. After controlling for age class and mass, jaw length was smaller in pregnant compared to non-pregnant yearlings and subadults, which suggests a trade-off between reproduction and growth. The bias towards females in yearlings increased as gestation proceeded, which suggests that the bias might be a result of selective abortion of male foetuses. Although results do not exclude an investment in males to increase number of grand-offspring, they suggest that young hinds may produce daughters as a trade-off between low energetic-cost offspring and their need to grow.Communicated by S. Krackow     

Climate and maternal effects modify sex ratios in a weakly dimorphic marsupial

There is growing evidence that the sex ratios of wild vertebrate populations are determined by mechanisms that are directly influenced by environmental characteristics. The Trivers–Willard (TWH) and extrinsic modification (EMH) hypotheses postulate differing determinants of mammalian offspring sex ratios. TWH states that mothers allocate resources according to their current condition and sex-specific offspring costs. EMH states that environmental forces that affect maternal condition determine offspring sex ratios, independently of maternal tactics of sex-biased allocation. We statistically assessed support for each of these hypotheses using long-term life histories of the allied rock-wallaby, Petrogale assimilis; a continuously breeding, polygynous, weakly dimorphic marsupial. We showed that birth sex ratios were equal and independent of maternal and environmental conditions. However, secondary sex ratios were male-biased under good environmental conditions and for high quality mothers or mothers in good condition. Sex differences in offspring survival contributed to these biases: (1) environmental conditions strongly influenced survival to pouch emergence (in support of EMH) and (2) maternal quality affected survival to the end of maternal care (in support of TWH). Environmental effects on survival were more important than maternal factors over the entire period of maternal care and contributed most to male-biased sex ratios at pouch emergence. In contrast, maternal mass was the best predictor of sex ratios at the end of maternal care—the life history stage where offspring body mass differed between the sexes.     

Communal nesting, kinship, and maternal success in a social primate

Communal nesting, where several mothers regularly pool and cooperatively rear offspring, is unusual in mammals. This type of crèching behavior is especially rare among primates, with the notable exceptions of humans, some nocturnal strepsirrhines, and—as we show in this study—black-and-white ruffed lemurs (Varecia variegata). Here, we combine data on nesting behavior, genetic relatedness, and infant survivorship to describe variation in ruffed lemur infant care and to examine the potential benefits of ruffed lemur communal breeding. Reproductive events were rare, and females produced litters (synchronously) only once in 6 years of observation. We show that not all mothers participate in communal crèches, but those that did had greater maternal success; communal breeders spent more time feeding and their offspring were more likely to survive. Although cooperating mothers were often related, females also cooperated with non-kin, and those who shared infant care responsibilities had greater maternal success than mothers who did not participate. If there is indeed a causal link between maternal cooperation and reproductive success, this unusual behavior, like that of human communal rearing, may have evolved via some combination of kin selection and mutualism.     

Variation in offspring sex ratio among individual Weddell seal (<Emphasis Type="Italic">Leptonychotes weddellii</Emphasis>) females of different quality

The Trivers–Willard model predicts that in polygynous species, superior-quality females will maximize their fitness by producing male offspring. Using a sample of 1,780 Weddell seal (Leptonychotes weddellii) pups recorded over 31 years, we investigated relationships between offspring sex ratio and maternal age, reproductive experience, an index of maternal lifetime reproductive output, and annual environmental variations. We found evidence that females with higher index of lifetime reproductive output were more likely to produce male than female offspring but found only weak evidence that large-scale environmental variations influenced sex ratios. Our results suggest that mothers manipulate offspring sex to maximize their own fitness, and inherent maternal quality may influence offspring sex. These findings support the Trivers–Willard sex-allocation model. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Lactation performance of guinea pigs (Cavia porcellus) does not respond to experimental manipulation of pup demands

To ensure proper development of young, mothers should react to offspring signals of need. Studies of such parent-offspring interaction often manipulated litter size to measure effects of changed offspring food demand. We used the extreme precociality of guinea pig (Cavia porcellus) pups to increase offspring demand without changing any other litter characteristic. As pups contribute to their own energy demands from birth by independent feeding, their food demand can be increased by withholding solid food early in lactation. We studied whether mothers reacted to increased food demand of offspring by enhanced parental care, especially by changes in the pattern of milk production and nursing. Pups deprived of solid food early in lactation grew more slowly and were in poorer body condition than pups in control litters, even after the former had access to solid food in late lactation. Mothers of deprived young reacted to offspring long-term need by maintaining nursing behaviour for longer than control mothers. However, this change in behaviour did not occur early in lactation when pup short-term need was greatest nor did it result in increased milk transfer at any time. Energy allocation of mothers measured by changes in their food intake, maternal body reserves, and milk production stayed the same whether offspring had early access to solid food or not. Thus mothers did not increase energy allocation to pups even though they apparently had information about the pups' poor state.     

Differential effects of offspring condition-dependent signals on maternal care regulation in the European earwig

Parent–offspring conflict theory predicts the evolution of offspring solicitation signals that can influence the amount and/or the duration of parental investment. Short-term effects of offspring solicitation signals on parental food provisioning have been widely demonstrated, but persistent effects of offspring signals on the maintenance of parental care have been rarely studied. Also, the relation between the amount of care provided to the brood and how it is distributed among individual offspring within a brood is not well enough understood. Here, we investigated in the European earwig (Forficula auricularia) the effects of offspring condition-dependent chemical signals on the maintenance of maternal care among broods and the distribution of maternal food within broods. Mothers were isolated from their brood for 3 days and continuously exposed to chemical signals extracted from broods of experimentally manipulated nutritional state. After re-introducing mothers to their brood, a range of maternal behaviours were quantified. We found that earwig mothers groomed their offspring significantly more after exposure to chemical extract from high-food brood in comparison with mothers exposed to extract from low-food brood, which in turn displayed significantly more aggressive behaviour. Furthermore, we manipulated offspring individual nutritional condition within the brood to evaluate the effect of offspring state on the within-brood food distribution. Within broods, poorly fed individuals received significantly more food than well-fed individuals, probably due to scramble competition. These results show that earwig nymphs express multi-component condition-dependent signals and behaviours differentially affecting maternal care provisioned to the brood and the distribution of care within broods.     

Prelaying maternal condition modifies the association between egg mass and T cell-mediated immunity in kestrels

Theoretical models of parental care predict differential allocation in relation to the expected fitness of the offspring. As birds must allocate all the resources required for embryonic development in self-contained packages, maternal egg allocation takes a central role in avian life histories. It is predicted that mothers can influence offspring performance by varying the size or composition of their eggs. In this context, T cell-mediated immune response has been revealed as a valuable tool to evaluate fledgling fitness. However, little is known about its relationships to egg mass. I describe a negative association between egg mass and cellular immune response in Eurasian kestrel nestlings (Falco tinnunculus) throughout 3 years. To explore how environmental conditions could mediate this relationship, I experimentally supplied food to females before egg formation in the third study year. I found that this relationship turned to positive in food-supplied females without any effect on egg size. This result shows that environmental conditions before egg formation mediate the relationship between egg mass and future immune response of the nestlings. I suggest that females may be constrained in improving the future immune response of their offspring due to resource allocation trade-offs determined by their pre-laying condition.     

Reproductive effort in relation to maternal social rank in reindeer (<Emphasis Type="Italic">Rangifer tarandus</Emphasis>)

In polygynous mammals, high-quality females may increase their fitness by providing superior care to their offspring. Based on the agonistic interactions of female reindeer in an experimental herd during two consecutive years (1997 and 1998), we tested whether maternal social rank influenced: (1) winter body-mass change of females, (2) preparturition reproductive effort (measured as fecundity, the birth mass and the birth date of their calves), (3) preweaning maternal effort (measured as calves preweaning mortality, early preweaning and late preweaning growth rate and September body mass of calves), and (4) postweaning maternal effort (measured as calves body-mass change during their first winter). In the models, we included September females body mass as a covariate to separate the effects of maternal rank and body mass. We also tested whether the effect of social rank on maternal efforts was dependent on offspring sex. High-ranked females gained body mass whereas low-ranked females lost weight during the winter. Fecundity was higher and date of birth was earlier in high-ranked females than in subordinates, whereas no effect of females rank on birth mass of calves was found. Early preweaning growth rate and September body mass of calves increased with increasing females social rank, whereas late preweaning daily growth rate of calves was not influenced by females rank. Calves preweaning mortality was only influenced by year, which also explained most of the variance in the winter body-mass change of calves. The effects of females rank on the reproductive-efforts parameters studied were not specific to offspring sex. These findings suggest that females rank influences reproductive effort during the preparturition, as well as the preweaning, period, the effect being sex independent.Communicated by R. Gibson     

Sibling competition in guinea pigs (<Emphasis Type="Italic">Cavia aperea</Emphasis> f. <Emphasis Type="Italic">porcellus</Emphasis>): scrambling for mother’s teats is stressful

Lactation is the most energy-intense period in the life of a female mammal. This can cause severe conflict between mother and offspring over the duration of lactation but also between siblings over the amount of milk each pup gets from its mother. Thus, competitive interactions between siblings are expected, and competition is likely to increase with litter size, particularly in species where the number of offspring exceeds the number of teats. We studied sibling competition in the domestic guinea pig (Cavia aperea f. porcellus), which has two teats, but frequently bears litters of up to five pups. By cross-fostering we created non-competition (control) litters with two pups and competition litters with four pups and observed nursing behaviour on days 5, 10, 15 and 20 postpartum. Pups of larger litters had lower growth rates, indicating increased competition among siblings in these litters. Pups of larger litters had to wait longer for access to a teat and spent less time suckling than pups of smaller litters but ate more solid food instead. Additionally, we manipulated the individual short-term need of pups by separating half of the pups of each litter for 2 h from their mothers before observation. Within a litter, hungry pups achieved access to milk faster and spent more time suckling than non-hungry pups. Pups competed mostly by scramble competition. Aggressive interactions occurred only in large litters. Pups of large litters had higher cortisol levels than pups in small litters. These effects decreased with age as pups became increasingly independent of maternal milk. Pup behaviour appears to fit better with models of scramble competition than with those of honest signalling. This contribution is part of the special issue “Sibling competition and cooperation in mammals” (guest editors: Robyn Hudson and Fritz Trillmich).     

Parent–offspring and sibling conflict in Galápagos fur seals and sea lions

Parent–offspring conflict theory is well supported by theoretical arguments. However, empirical observations are often difficult to interpret and have contradicted one of its most appealing predictions that parent and offspring should disagree over killing of nest or littermates. We present the first examples of deadly conflict between siblings of different cohorts. In Galápagos fur seals (Arctocephalus galapagoensis) and sea lions (Zalophus wollebaeki), mothers often wean their single offspring at 2 years. This leads to a situation where up to 23% of all pups are born while the older sibling is still being nursed. Younger siblings are disadvantaged by being born lighter than neonates without older still dependent siblings. Pups born while an older sib is still dependent grow less in early life (fur seal) and suffer increased early mortality (both species) through direct aggression or scramble competition with the older sibling. This effect is much stronger in years of high sea surface temperature (El Niño) indicating low marine productivity and if the older offspring is a male. In both species, mothers interfere aggressively in this conflict by defending the younger offspring. In years of El Niño, intense resistance to maternal aggression by the older offspring happens frequently in the fur seal. Such resistance against weaning can induce maternal neglect of the newborn. Given substantial year to year variation in offspring growth, maternal aggression forces weaning in the older sibling only if it has reached sufficient size to support itself by foraging. In Galápagos fur seals, pups with older siblings can either represent insurance against loss of older offspring or extra reproductive value.     

Female-biased sex allocation of offspring by an <Emphasis Type="Italic">Apodemus</Emphasis> mouse in an unstable environment

We investigated the effects of population fluctuation on the offspring’s sex allocation by a weakly polygynous mouse, Apodemus argenteus, for 3 years. In acorn-poor seasons, heavier mothers invested more in sons, and lighter mothers invested more in daughters. In acorn-rich seasons, heavier mothers invested more in daughters, and lighter mothers invested more in sons. Maternal body condition and litter size affected the sex allocation. Furthermore, there was a maternal investment trade-off between a son’s birth mass and the number of daughters. Based upon the effect of population fluctuation on the lifetime reproductive success of each sex, we proposed the new “safe bet hypothesis”. This hypothesis predicts that frequent and unpredictable change in female distribution, which is often caused by abrupt fall in food condition, favors female-biased maternal investment to offspring by polygynous mammals and is applicable to many small mammals inhabiting in unstable environments.     

Inbreeding-based bias in parental responsiveness to litters of oldfield mice

This study investigated variation in parental behavior in oldfield mice (Peromyscus polionotus). Specifically, I examined the possibility that parental behavior and probability of litter loss may differ depending on whether parents are related to one another and, therefore, whether offspring are inbred. When parents are related, they share more genes with their offspring and so may be predicted to invest more in inbred offspring if these offspring do not inherently have a greater risk of juvenile mortality. Survival of inbred pups did not differ from survival of outbred pups, and females tended to exhibit a preference, in the form of enhanced parental care, for inbred litters. Males did not display any consistent preferences. Inbred litters were left unattended more often during the immediate post-partum period than were outbred litters, but this inconsistent finding appeared to have a smaller effect than the overall improved maternal care provided to inbred litters. Females thus appeared to modulate their behavior to a greater degree than did males depending on characteristics of the litter. Patterns of litter loss indicated that complete death of litters was independent of litter inbreeding, whereas loss of selected pups in a litter occurred significantly more often when litters were inbred. Complete and partial loss of litters may be functionally different behaviors that are triggered by different cues. Received: 20 September 1996 / Accepted after revision: 28 April 1997     

Benefits and costs of earwig (Forficula auricularia) family life

The evolution of parental care and family group formation critically depends on offspring survival benefits and parental fecundity costs of care under given ecological conditions. Investigations of the functional significance of care in insect species that exhibit facultative parental care have been relatively rare but may be of particular interest for better understanding of benefit and cost schedules at an early evolutionary stage. In this study, aspects of benefits and costs of care were addressed in the sub-social European earwig (Forficula auricularia; Dermaptera: Forficulidae) by manipulating the presence of tending mothers and brood size in a fully crossed experimental design. Larvae growing in broods tended by their mother or of reduced size showed a higher survival probability than larvae growing in untended or large broods, as predicted if maternal care is beneficial and shaped by a trade-off between number and quality of offspring. Analysis of patterns of food consumption and developmental time further suggested that the benefit of maternal attendance is mediated by the maternal provisioning of food, while the quality–quantity trade-off seemed to be driven by sibling rivalry. Further, tending mothers delayed the production of a second clutch, indicating a potential cost of care in terms of lifetime fecundity. This study experimentally shows benefits and potential costs of maternal care and family group formation in the European earwig. More detailed behavioural experiments will be required to fully understand how behavioural interactions among family members mediate these reproductive outcomes.