Maintenance of Multifemale Social Organization in a Group of <Emphasis Type="Italic">Nomascus concolor</Emphasis> at Wuliang Mountain,Yunnan, China

Many short-term studies have reported groups of black crested gibbons containing ≥2 adult females (Nomascus concolor). We report the stability of multifemale groups in this species over a period of 6 yr. Our focal group and 2 neighboring groups included 2 breeding females between March 2003 and June 2009. We also habituated 1 multifemale group to observers and present detailed information concerning their social relationships over a 9-mo observation period. We investigated interindividual distances and agonistic behavior among the 5 group members. The spatial relationship between the 3 adult members (1 male, 2 females) formed an equilateral triangle. A subadult male was peripheral to the focal group, while a juvenile male maintained a closer spatial relationship with the adult members. We observed little agonistic behavior among the adult members. The close spatial relationship and lack of high rates of agonistic behavior among females suggest that the benefits of living in a multifemale group were equal to or greater than the costs for both females, given their ecological and social circumstances. The focal group occupied a large home range that was likely to provide sufficient food sources for the 2 females and their offspring. Between March 2003 and June 2009, 1 adult female gave 2 births and the other one gave 1 birth. All individuals in the focal group survived to June 2009. A long-term comparative study focused on females living in multifemale groups and females living in pair-living groups would provide insight into understanding the evolutionary mechanisms of the social system in gibbons.     

Hormonal manipulation of offspring number: maternal effort and reproductive costs

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

Life History and Reproductive Strategies of Khao Yai <Emphasis Type="Italic">Hylobates lar</Emphasis>: Implications for Social Evolution in Apes

Among primates, great apes have the most extended life histories and they also appear socially specialized because of their flexible association patterns and sociosexual relationships. Researchers have hypothesized that such subtle social commonalities in combination with a slow life pace lead to great apes advanced cognition. Small apes, in contrast to great apes, are commonly believed to be socially inflexible, and little comparative life history data exist for wild populations. We investigated how the small white-handed gibbon (Hylobates lar) fits into a great ape life history and sociality framework. We followed the life histories of adults in 12 groups over ca. 18 yr at Khao Yai National Park, Thailand. Results demonstrate that the life histories of white-handed gibbons closely resembled those of other apes. Mean female age at first reproduction was late (11.06 yr), and mean interbirth interval (41 ± 9.1 mo) and juvenile period (9.5 ± 1.8 yr) were long. Multimale grouping of 2 adult males and 1 female was a common alternative (21.2% groups) to the traditional hylobatid pair-living social organization in our population. Female sexual partnerships include a variety of polyandrous mating strategies for both pair-living females and females in multimale groups. From our long-term study a picture of social complexity materializes that resembles social complexities in other apes. In conclusion, we infer that gibbons share commonalities postulated to unite great apes based on similar life histories and very flexible social and sexual relationships.     

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.     

Sterile pyuria in a population of wild white‐handed gibbons (Hylobates lar)

Urinalysis is an emerging method for monitoring the health and energy balance of wild primates. Here, we report the first urinalysis of wild gibbons. We used multi‐reagent test strips to monitor the health status of 52 individual white‐handed gibbons (Hylobates lar) inhabiting Khao Yai National Park, Thailand. Most urinary reference values were within normal ranges; however, regardless of age‐ and sex‐class or monthly fruit productivity, we found unexpectedly high rates of urinary leukocytes (50% and 90% of individuals in 2001–2003 and 2006, respectively). In contrast to previous studies of African apes, this finding is coupled with the near absence of urinary nitrites, demonstrating pervasive levels of sterile pyuria. This result is the first reported case of sterile pyuria in a population of wild primates. The etiology of human sterile pyuria is diverse, but in all cases it is diagnostic of systemic inflammation. We discuss the potential causes of sterile pyuria in the gibbons of Khao Yai. Am. J. Primatol. 71:880–883, 2009. © 2009 Wiley‐Liss, Inc.     

Heterogeneity in individual quality overrides costs of reproduction in female reindeer

Reproductive allocation at one age is predicted to reduce the probability of surviving to the next year or to lead to a decrease in future reproduction. This prediction assumes that reproduction involves fitness costs. However, few empirical studies have assessed whether such costs may vary with the age at primiparity or might be overridden by heterogeneities in individual quality. We used data from 35 years’ monitoring of individually marked semi-domestic reindeer females to investigate fitness costs of reproduction. Using multi-state statistical models, we compared age-specific survival and reproduction among four reproductive states (never reproduced, experienced non-breeders, reproduced but did not wean offspring, and reproduced and weaned offspring) and among contrasted age at primiparity. We assessed whether reproductive costs occurred, resulting in a trade-off between current reproduction and future reproduction or survival, and whether early maturation was costly or rather reflected differences in individual quality of survival and reproduction capabilities. We did not find any evidence for fitness costs of reproduction in female reindeer. We found no cost of gestation and lactation in terms of future reproduction and survival. Conversely, successful breeders had higher survival and subsequent reproductive success than experienced non-breeders and unsuccessful breeders, independently of the age at primiparity. Moreover, it was beneficial to mature earlier, especially for females that successfully weaned their first offspring. Successful females at early primiparity remained successful throughout their life, clearly supporting the existence of marked among-female differences in quality. The weaning success peaked for multiparous females and was lower for first-time breeders, indicating a positive effect of experience on reproductive performance. Our findings emphasize an overwhelming importance of individual quality and experience to account for observed variation in survival and reproductive patterns of female reindeer that override trade-offs between current reproduction and future performance, at least in the absence of harsh winters.     

Infant loss during and after male replacement in gibbons

According to the sexual selection hypothesis, infanticide during resident male replacement is an adaptive strategy that has evolved because the killing of unweaned offspring sired by previous males shortens the inter‐birth intervals of the mothers whose infants are targeted and thereby increases the reproductive fitness of the perpetrator. To test this hypothesis, we describe previously unreported cases of primary male replacement for two gibbon species (Hylobates lar and Nomascus nasutus), and review all other reported cases of primary male replacement in gibbons. Overall, infants were present in nearly half of all cases (16/33, 48%) and of the 18 infants present during replacement, 50% (N = 9) disappeared within 2 months of the event. In four of the five cases where there was sufficient demographic information to identify the likely sire of the subsequent offspring of females that lost infants, the new male was believed to be the sire. Infants were also less likely to die or disappear if the new male and original resident male were possible kin. However, there was no significant difference in the age of infants between those that died or disappeared following replacement and those that survived to weaning (p = .630). Our review of takeover‐related infant loss in gibbons confirms that periods of male instability are risky for unweaned infants and that replacing males benefit from infant loss. Nevertheless, variability in the context of infant loss and difficulties related to data collection in the field make it difficult to test competing hypotheses concerning the mechanisms and functions of infanticide in the small apes.     

Experimental field studies of Asian ape social systems

The Asian apes, orangutans and gibbons, possess unusual social systems among anthropoid primates. Social groups of gibbons consist of mated adult pairs and their offspring; mature orangutans are primarily solitary. Recent experimental field research has begun to yield insights into the behavioral mechanisms employed by these animals to maintain their characteristic patterns of social dispersion. While spatial separation between female orangutans appears to be maintained passively, aggression, which is manifest during direct encounters and long-distance vocal interactions, mediates male asociality. Male-male aggression is the result of intense intrasexual competition occurring between animals for mating access to females. To reduce intrasexual competition, male orangutans have adopted alternative mating tactics. In contrast to female orangutans, female gibbons show marked agonistic tendencies toward conspecifics. Female territoriality contributes to preventing males from becoming polygynous. Male gibbons, restricted to monogamous relationships, attempt to ensure their paternity through intrasexual aggression. These observations suggest that the spatial dispersion of females constrains male mating options in both species. However, variations between orangutan and gibbon social systems can be understood as consequences of the temporal dispersion of sexually receptive females. The temporal clumping of females, due to relatively high operational sex ratios, limits the ability of male gibbons to acquire multiple mates. Conversely, an extremely low operational sex ratio in orangutans creates a strong selection pressure for intrasexual competition and polygamous mating. These considerations provide a novel framework for interpreting the social systems of the African apes.     

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.     

Social organization, reproduction and rearing strategies of Callimico goeldii: new clues from the wild

The callitrichines are a specialized radiation of primates that are characterized in part by variable social systems and cooperative infant care. Callimico goeldii, unlike the other callitrichines, have single rather than twin offspring, reducing the need for allocare and permitting synchronous breeding within groups. Low mortality rates among offspring and unstable social groups are suggested to be possible factors that have led to single births among C. goeldii. Single offspring may benefit from greater maternal investment and more frequent food sharing than twin offspring, factors that may help to explain why C. goeldii reaches sexual maturity more rapidly than other callitrichines. In addition, increased breeding opportunities for young C. goeldii females may have selected for rapid maturation rates among this species. Postpartum ovulation and aseasonal resource availability appear to permit females to have biannual birth seasons, further increasing the potential reproductive output.     

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.     

Female red squirrels fit Williams' hypothesis of increasing reproductive effort with increasing age

Williams predicted that reproductive effort should increase as individuals age and their reproductive value declines. This simple prediction has proven difficult to test because conventional measures of energy expenditure on reproduction may not be a true reflection of reproductive effort. We investigated age-specific variation in female reproductive effort in a stable population of North American red squirrels where energy expenditure on reproduction is likely to reflect actual reproductive effort. We used seven measures of reproductive effort spanning conception to offspring weaning. We found that females completed growth by age 3 and that reproductive value decreased after this age likely because of reproductive and survival senescence. We therefore, predicted that reproductive effort would increase from age 3 onwards. The probability of breeding, litter mass at weaning, and likelihood of territory bequeathal were all lower for 1- and 2-year-old females than for females older than 3 years, the age at which growth is completed. That growing females are faced with additional energetic requirements might account for their lower allocation to reproduction as compared with older females. The probability of attempting a second reproduction within the same breeding season and the propensity to bequeath the territory to juveniles increased from 3 years of age onwards, indicating an increase in reproductive effort with age. We think this increase in reproductive effort is an adaptive response of females to declining reproductive values when ageing, thereby supporting Williams' prediction.     

Maternal effects and their consequences for offspring fitness in the Yellow Dung Fly

1. Maternal adult diet and body size influence the fecundity of a female and possibly the quality and the performance of her offspring via egg size or egg quality. In laboratory experiments, negative effects in the offspring generation have often been obscured by optimal rearing conditions.
2. To estimate these effects in the Yellow Dung Fly, Scathophaga stercoraria , how maternal body size and adult nutritional status affected her fecundity, longevity and egg size were first investigated.
3. Second, it was investigated how female age and adult nutritional experience, mediated through the effects of egg size or egg quality, influenced the performance of offspring at different larval densities.
4. Maternal size was less important than maternal adult feeding in increasing reproductive output. Without food restriction, large females had larger clutch sizes and higher oviposition rates, whereas under food restriction this advantage was reversed in favour of small females.
5. Offspring from mothers reared under nutritional stress experienced reduced fitness in terms of egg mortality and survival to adult emergence. If the offspring from low-quality eggs survived, the transmitted maternal food deficiency only affected adult male body size under stressful larval environments.
6. Smaller egg sizes due to maternal age only slightly affected the performance of the offspring under all larval conditions.     

Survival costs of reproduction predict age-dependent variation in maternal investment

Life-history theory predicts that older females will increase reproductive effort through increased fecundity. Unless offspring survival is density dependent or female size constrains offspring size, theory does not predict variation in offspring size. However, empirical data suggest that females of differing age or condition produce offspring of different sizes. We used a dynamic state-variable model to determine when variable offspring sizes can be explained by an interaction between female age, female state and survival costs of reproduction. We found that when costs depend on fecundity, young females with surplus state increase offspring size and reduce number to minimize fitness penalties. When costs depend on total reproductive effort, only older females increase offspring size. Young females produce small offspring, because decreasing offspring size is less expensive than number, as fitness from offspring investment is nonlinear. Finally, allocation patterns are relatively stable when older females are better at acquiring food and are therefore in better condition. Our approach revealed an interaction between female state, age and survival costs, providing a novel explanation for observed variation in reproductive traits.     

Begging for information: mother-offspring food sharing among wild Bornean orangutans

Transfer of solid food from mothers or other adults to dependent offspring is commonly observed in various primate species and both nutritional and informational benefits have been proposed to explain the function of such food sharing. Predictions from these hypotheses are tested using observational data on wild orangutans (Pongo pygmaeus wurmbii) at Tuanan, Central Borneo, Indonesia. In 1,145 hr of focal observation and 458 recorded food interactions between four pairs of females with offspring it was found that virtually all transfers were initiated by the offspring and that younger infants solicited food more often and did so for a greater variety of items than older offspring. All offspring primarily solicited food that was difficult to process, i.e., inaccessible to them. Furthermore, the amount of food solicitation was negatively correlated with ecological competence. Hence food sharing seemed to be related to an offspring's skill level, as suggested by the informational hypothesis. In contrast, offspring did not solicit high-quality items more than low-quality items and food sharing did not peak around the age of weaning, as predicted by the nutritional hypothesis. Mothers were usually passively tolerant, allowing offspring to take food but hardly ever provisioned. Parent-offspring conflict concerning food sharing was only observed well after weaning. Thus, by taking food directly from the mother, young orangutans were able to obtain information about the affordances and nutritional value of food items that were otherwise out of their reach and could familiarize themselves with the mother's diet. In species such as orangutans or other apes, characterized by a broad diet that requires extractive foraging, informational food transfer may be vital for an immature to acquire complex feeding skills and adult diet.     

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.     

Senescence and costs of reproduction in the life history of a small precocial species

Species following a fast life history are expected to express fitness costs mainly as increased mortality, while slow‐lived species should suffer fertility costs. Because observational studies have limited power to disentangle intrinsic and extrinsic factors influencing senescence, we manipulated reproductive effort experimentally in the cavy (Cavia aperea) which produces extremely precocial young. We created two experimental groups: One was allowed continuous reproduction (CR) and the other intermittent reproduction (IR) by removing males at regular intervals. We predicted that the CR females should senesce (and die) earlier and produce either fewer and/or smaller, slower growing offspring per litter than those of the IR group. CR females had 16% more litters during three years than IR females. CR females increased mass and body condition more steeply and both remained higher until the experiment ended. Female survival showed no group difference. Reproductive senescence in litter size, litter mass, and reproductive effort (litter mass/maternal mass) began after about 600 days and was slightly stronger in CR than IR females. Litter size, litter mass, and offspring survival declined with maternal age and were influenced by seasonality. IR females decreased reproductive effort less during cold seasons and only at higher age than CR females. Nevertheless, offspring winter mortality was higher in IR females. Our results show small costs of reproduction despite high reproductive effort, suggesting that under ad libitum food conditions costs depend largely on internal regulation of allocation decisions.     

The tempo of human childhood: a maternal foot on the accelerator,a paternal foot on the brake

Relative to the life history of other great apes, that of humans is characterized by early weaning and short interbirth intervals (IBIs). We propose that in modern humans, birth until adrenarche, or the rise in adrenal androgens, developmentally corresponds to the period from birth until weaning in great apes and ancestral hominins. According to this hypothesis, humans achieved short IBIs by subdividing ancestral infancy into a nurseling phase, during which offspring fed at the breast, and a weanling phase, during which offspring fed specially prepared foods. Imprinted genes influence the timing of human weaning and adrenarche, with paternally expressed genes promoting delays in childhood maturation and maternally expressed genes promoting accelerated maturation. These observations suggest that the tempo of human development has been shaped by consequences for the fitness of kin, with faster development increasing maternal fitness at a cost to child fitness. The effects of imprinted genes suggest that the duration of the juvenile period (adrenarche until puberty) has also been shaped by evolutionary conflicts within the family.     

Varying Ecological Quality Influences the Probability of Polyandry in White-handed Gibbons (Hylobates lar) in Thailand

Although members of the family Hylobatidae are known to be monogamous, adult white-handed gibbons ( Hylobates lar ) at Khao Yai National Park, Thailand, also show multimale groups and polyandry. A need for more than one male to successfully raise offspring cannot explain the occurrence of polyandry in these territorial primates, because direct paternal care is absent in this species. We hypothesize that polyandry is primarily related to costs/benefits for males of cooperatively defending a female and/or resources; our prediction was that polyandry would become more frequent with increasing costs of female/resource defense. We measured the ecological quality of seven gibbon home ranges over a 3-yr period (2001–2003) to investigate how resource availability affected the probability of polyandry, and found a significant negative relationship between home range quality and home range size. Larger home ranges were of lower quality. As predicted, groups living on larger, poorer home ranges also experienced longer periods of polyandry. In forest areas of comparatively low quality, acquiring and maintaining a large home range that includes enough resources for a female to reproduce steadily may surpass a single male's capacity. Our model of cooperative male polyandry was supported by preliminary data of shared territorial defense and access to the female. However, interaction proportions were strongly skewed, and female's primary male partners monopolized grooming and mating. Nevertheless, a primary male on a large territory may benefit from the presence of a secondary male with aid in territorial/female defense, whereas a secondary male may gain by avoiding high dispersal costs.     

Phenotypic plasticity in Daphnia magna Straus: variable maturation instar as an adaptive response to predation pressure

Life history responses of four Daphnia magna clones at two food levels were studied to assess the importance of maturation instar on the plasticity of fitness responses under simulated mortality regimes. Females of the clones studied could vary offspring size with consequent effects on their maturation time. Significant genetic variability in life history and fitness responses, measured as the intrinsic rate of population increase, within and across food levels was observed, but most of this variation could be attributed to maturation instar differences among clones within and across environments. In the laboratory, without extrinsic mortality, females maturing earlier always had higher fitness than those maturing later, indicating a clear fitness cost of delaying maturity. Nevertheless using a model, we showed that the observed maturation instar effects on life history responses can lead to differences in fitness under different size-selective predation regimes, such that females with delayed maturity have higher fitness under invertebrate predation while females maturing earlier have higher fitness under fish predation regimes. These results suggest that intraclonal variation in offspring size and hence in the number of maturation instars can be an adaptation to living in habitats subject to temporal fluctuations in fish and invertebrate predation pressure.