The effect of prey abundance and foraging tactics on the population dynamics of a social, territorial carnivore, the spotted hyena

We used naturally occurring spatial and temporal changes in prey abundance to investigate whether the foraging behavior of a social, territorial carnivore, the spotted hyena ( Crocuta crocuta ), conformed to predictions derived from the ideal free distribution. We demonstrate that hyenas in the Ngorongoro Crater, Tanzania, redistributed themselves from less profitable to more profitable areas, even when this required them to undertake foraging trips to areas beyond their clan territory boundary, or required normally philopatric females to emigrate. As expected for a system with rank related access to food resources in the territory, females of low social status foraged more often outside their territory and were more likely to emigrate than dominant females. Probably because Crater hyenas regularly foraged outside their territories, there was no correlation between clan size and prey density within territories, suggesting that clan sizes may have exceeded the carrying capacity of territories. A substantial decline of the hyena population in the Crater from 385 adults in the mid 1960s to 117 in 1996 was most likely due to a substantial decline of their main prey. The decline in the hyena population was associated with a decline in the size of clans but not in the number of clans. The number of clans probably remained constant due to emigration by females from large clans into vacant areas or clans with no adult females, and because hyenas regularly fed in areas containing concentrations of prey beyond their territory boundary. Between 1996 and 2003 annual recruitment rates of Crater hyenas consistently exceeded annual mortality rates, resulting in an almost doubling of the adult population. This increase was most likely due to an increase in prey abundance, a relatively low level of predation on hyenas by lions ( Panthera leo ), and an absence of high levels of disease related mortality.     

A Test of the Cross-Generational Transmission of Grooming Preferences in Macaques

In this study we compared the grooming networks of macaque mothers and adult daughters in order to test whether primate social preferences may be transmitted from one generation to the next. We studied four social groups belonging to three different species (Macaca fascicularis, M. fuscata and M. sylvanus). We found no evidence for the transmission of individual degrees of kin bias or of preference for high‐ranking individuals (transmission of ‘rules of choice’). Only in one of four social groups were idiosyncratic interindividual preferences of mothers significantly similar to those of their adult daughters. Overall, the results of this study question the generality of the intergenerational transmission of social preferences in macaques. It is suggested that species‐specific degrees of preferences for kin and for high‐ranking individuals should be selected for and strategically adjusted by individual females in relation to social circumstances.     

The maternal social environment shapes offspring growth,physiology, and behavioural phenotype in guinea pigs

Background

Prenatal conditions influence offspring development in many species. In mammals, the effects of social density have traditionally been considered a detrimental form of maternal stress. Now their potential adaptive significance is receiving greater attention.Sex-specific effects of maternal social instability on offspring in guinea pigs (Cavia aperea f. porcellus) have been interpreted as adaptations to high social densities, while the effects of low social density are unknown. Hence, we compared morphological, behavioural and physiological development between offspring born to mothers housed either individually or in groups during the second half of pregnancy.

Results

Females housed individually and females housed in groups gave birth to litters of similar size and sex-ratios, and there were no differences in birth weight. Sons of individually-housed mothers grew faster than their sisters, whereas daughters ofgroup-housed females grew faster than their brothers, primarily due to an effect on growth of daughters. There were few effects on offspring behaviour. Baseline cortisol levels in saliva of pups on day 1 and day 7 were not affected, but we saw a blunted cortisol response to social separation on day 7 in sons of individually-housed females and daughters of group-housed females. The effects were consistent across two replicate experiments.

Conclusions

The observed effects only partially support the adaptive hypothesis. Increased growth of daughters may be adaptive under high densities due to increasedfemale competition, but it is unclear why growth of sons is not increased under low social densities when males face less competition from older, dominant males. The differences in growth may be causally linked to sex-specific effects on cortisol response, although individual cortisol response and growth were not correlated, and various other mechanisms are possible. The observed sex-specific effects on early development are intriguing, yet the potential adaptive benefits and physiological mechanisms require further study.

     

Maternal rank is not correlated with cub survival in the spotted hyena, Crocuta crocuta

Reproductive success in female spotted hyenas, Crocuta crocuta,is positively correlated with social rank. High-ranking femalesare known to produce more offspring, but the effects of maternalrank on early cub survivorship have not been investigated. Cubmortality was examined over a 4-year period in one clan of wild-livingspotted hyenas in Kenya. Data were obtained for 100 cubs in63 litters produced by 27 adult females. Survivorship of cubsfrom birth through their first year was examined as a functionof litter size, sex of cubs, and maternal rank. Overall, cubmortality was high (61%). Contrary to expectation, singletoncubs did not survive better than twins, and there was no differencein survivorship between female and male cubs. High-ranking motherswere not more successful at raising twins or daughters thanwere low-ranking mothers. There was no correlation between cubmortality and maternal rank. Peaks in cub mortality coincidedwith life stage events, including mean age of arrival at a communalden, and age at which cubs began visiting kills. Documentedcauses of mortality included intraclan infanticide, disease,orphaning, predation by lions, and a mechanism of filial infanticidethat has not been previously described in this species: selectivelitter reduction by mothers via partial litter abandonment.No instances of facultative or obligate siblicide were detected.During this study, association between rank and number of cubssurviving to 1 year of age appeared to be due to differencesin reproductive output and not differential survival of cubswithin their first year.     

Behavioral role differentiation in the primitively eusocial waspBelonogaster juncea juncea (Hymenoptera: Vespidae)

With a view toward describing behavioral variability among individuals of the primitively eusocial speciesBelonogaster juncea juncea, we recorded the time-activity budget spent on five behavioral categories (foraging, building, feeding, inactivity, and reproduction) by 52 individuals belonging to four postemergence colonies. A principal-components analysis coupled with a hierarchical cluster analysis enabled us to discern four behavioral roles. The reproductive role is reserved to one individual (functional monogyny) and the workers’ role is differentiated into foragers, builders, and guards. The foragers are females that spend the most time (82.6% of their time) foraging, supplying the nest with prey load and liquid matter. The builders are individuals (with 41.5% of their time off the nest) that tend to bring pulp into the nest and then undertake building activities. The guards are those females that spend the most time (79.7% of their time) being inactive on the nest.     

Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas.

Little is known about to what extent the sensitivity of the hypothalamic-pituitary-adrenal (HPA) axis may be state dependent and vary in the same species between environments. Here we tested whether the faecal corticosteroid concentrations of matrilineal adult female spotted hyenas are influenced by social and reproductive status in adjacent ecosystems and whether they vary between periods with and without social stress. Females in the Serengeti National Park frequently become socially subordinate intruders in other hyena territories by undertaking long-distance foraging trips to migratory herds, whereas in the Ngorongoro Crater they usually forage inside their own small territories on resident prey. The faecal corticosteroid concentrations in Serengeti females were significantly higher than in Ngorongoro females. Energy expenditure by lactation is exceptionally high in spotted hyenas and this may be reflected in their corticosteroid levels. The faecal corticosteroid levels in both populations were higher in lactating than in non-lactating females. During periods of social stability, faecal corticosteroid concentrations increased in non-lactating females but not in lactating females as social status declined. Lactating Serengeti females had significantly higher faecal corticosteroid concentrations during periods with acute severe social stress than during periods without, indicating that the HPA axis is sensitive to social stimuli even in lactating females. So far few studies have used non-invasive monitoring methods for assessing social stress in freeranging animals. This study demonstrates for the first time, to the authors' knowledge, that corticosteroid concentrations may differ between periods with and without social stress for a free-ranging female mammal and that the modulating effect of social status may depend on reproductive status.     

Adaptive maternal cannibalism in snakes (Epicrates cenchria maurus, Boidae)

In many animal species, mothers that produce stillborn offspring or undeveloped ova immediately ingest them. This cannibalism has been interpreted in two ways: (1) as a form of parental care (to prevent disease spreading to healthy littermates, and eliminate predator-attracting scent cues); or (2) to recycle otherwise wasted energy, thus facilitating maternal recovery. Our experimental study on captive Colombian rainbow boas ( Epicrates cenchria maurus ) provides the first quantitative support for this latter hypothesis. We show that by eating their non-viable offspring and undeveloped eggs, female boas can rapidly recycle a significant component of their otherwise wasted reproductive investment. Female boas that ingested non-viable progeny equivalent to half their litter mass exhibited rapid recovery of dorsal musculature and hence were able to constrict prey items more forcefully than were unfed females when tested 2 weeks after parturition. The consequent enhancement of constricting ability may influence maternal survival and foraging success. Thus, maternal cannibalism may be an effective tactic to avoid wasting reproductive resources, and to shorten the period required for recovery from pregnancy.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 767–774.     

Prenatal Chemosensory Learning by the Predatory Mite Neoseiulus californicus

Background

Prenatal or embryonic learning, behavioral change following experience made prior to birth, may have significant consequences for postnatal foraging behavior in a wide variety of animals, including mammals, birds, fish, amphibians, and molluscs. However, prenatal learning has not been previously shown in arthropods such as insects, spiders and mites.

Methodology/Principal Findings

We examined prenatal chemosensory learning in the plant-inhabiting predatory mite Neoseiulus californicus. We exposed these predators in the embryonic stage to two flavors (vanillin or anisaldehyde) or no flavor (neutral) by feeding their mothers on spider mite prey enriched with these flavors or not enriched with any flavor (neutral). After the predators reached the protonymphal stage, we assessed their prey choice through residence and feeding preferences in experiments, in which they were offered spider mites matching the maternal diet (neutral, vanillin or anisaldehyde spider mites) and non-matching spider mites. Predator protonymphs preferentially resided in the vicinity of spider mites matching the maternal diet irrespective of the type of maternal diet and choice situation. Across treatments, the protonymphs preferentially fed on spider mites matching the maternal diet. Prey and predator sizes did not differ among neutral, vanillin and anisaldehyde treatments, excluding the hypothesis that size-assortative predation influenced the outcome of the experiments.

Conclusions/Significance

Our study reports the first example of prenatal learning in arthropods.     

Age,reproductive value,and dominance-related behaviour in vervet monkey females: cross-generational influences on social relationships and reproduction

Behavioural interactions among captive socially-living adult female vervet monkeys were analysed to determine whether (1) the motivation to maintain and increase, dominance rank declines with age as individual reproductive value declines, or (2) the cross-generational inheritance of dominance rank causes adult females to continue to involve themselves in dominance-related behaviours for the benefit of their daughters, even though their own reproductive value, is declining. The results indicate that adult females do not reduce their involvement in aggressive and dominance-related behaviours as they age. There was strong support for the hypothesis that older adult females maintain affiliative and supportive ties with their adult daughters, and that the daughters benefit from this relationship both in terms of social relationships and reproductive success. Young adult females without mothers were the recipients of more aggression, were less likely to be defeded when they were attacked and were less likely to challenge the rank of others compared to females with mothers living in the group. Young adult females with mothers produced significantly more surviving offspring and had a lower level of infant mortality than comparable adult females without mothers.     

Behavioral Profiles Related to Dominance Hierarchy in Associated Foundresses of Belonogaster juncea juncea (F.) (Hymenoptera: Vespidae)

This study was conducted to examine the phenomenon of task partitioning among associations of foundresses of the primitively eusocial wasp Belonogaster juncea juncea (F.). The time–activity budget for five main behavioral categories (foraging, building, feeding, inactivity, and reproduction) for each foundress belonging to trigynic associations was recorded using the instantaneous scanning technique. After ranking the individuals on the basis of agonistic encounters, data were submitted to a canonical discriminant analysis. The results show behavioral differences between individuals of each rank. The proportion of time allocated to foraging behavior is a good rank index. The females of the first rank spent less time on foraging behavior and significantly more time (13.6% of their time) on reproductive behavior than females of other ranks. The females of the second rank also spent less time on foraging behavior and showed a tendency toward building behavior. The females of the third rank spent significantly more time (77.28% of their time) on foraging behavior. The behavioral profile of each foundress was therefore determined by its rank on the dominance scale.     

Social Relationships Among Ring-Tailed Lemurs (Lemur catta) in Two Free-Ranging Troops at Berenty Reserve, Madagascar

We observed two free-ranging troops of ring-tailed lemurs at the Berenty Reserve, Madagascar. Kinship affinities in these troops are known only for mothers and their offspring 4 years of age. We attempted to quantify social relationships. Almost all agonistic interactions were dyadic, and triadic agonistic interactions, such as alliances, were very rare. Dominance hierarchies in both sexes in the two troops were not linear. As in cercopithecine monkeys, mothers were dominant over their adult daughters. However, the daughters were not ranked immediately below their mothers. Close proximity and social grooming occurred more frequently between closely related females, such as mother–daughter and sister–sister dyads, than between unrelated females. Frequent-proximity relations also occurred between adult males that had emigrated from another troop and entered the present troop together, even though they did not rank closely to one another. Subordinates were likely to groom and to greet dominants more frequently than vice versa. During group encounters, particular females were involved in agonistic interactions with animals of other troops, regardless of dominance rank. Adult males, regardless of their dominance rank, but not adult females, constantly tried to drive solitary males away.     

The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus)

It is widely accepted that natal philopatry is a prerequisite for the evolution of sociality. The life-history hypothesis maintains that longevity of adults results in extended territory tenure and thus limits breeding vacancies for offspring, which makes natal philopatry more likely. Here, we tested the importance of longevity for natal philopatry in females of a basal primate, the grey mouse lemur (Microcebus murinus). This species is regarded as being solitary due to its foraging habits but while males disperse, female offspring in this species forgo dispersal and form long-term sleeping groups with their mothers. We tested whether high adult survival could be a cause for natal philopatry of female offspring. In addition, we assessed costs and benefits associated with space sharing between mothers and daughters and whether mothers actively increase survival of daughters by beqeauthal of territories, information transfer about resources or thermoregulation. Contrary to our predictions, adult females had low-survival rates. Space sharing appeared to improve survival of both, mothers and daughters. This could be a result of information transfer about sleeping sites and thermoregulatory benefits. Our results cast doubt on the idea that longevity predisposes species for social traits and provide support for benefits of philopatry.     

How feeding competition determines female chimpanzee gregariousness and ranging in the Taï National Park, Côte d'Ivoire

Socioecological theory suggests that feeding competition shapes female social relationships. Chimpanzees (Pan troglodytes) live in fission–fusion societies that allow them to react flexibly to increased feeding competition by forming smaller foraging parties when food is scarce. In chimpanzees at Gombe and Kibale, female dominance rank can crucially influence feeding competition and reproductive success as high‐ranking females monopolize core areas of relatively high quality, are more gregarious, and have higher body mass and reproductive success than low‐ranking females. Chimpanzee females in Taï National Park do not monopolize core areas; they use the entire territory as do the males of their community and are highly gregarious. Although female chimpanzees in Taï generally exhibit a linear dominance hierarchy benefits of high rank are currently not well understood. We used a multivariate analysis of long‐term data from two Taï chimpanzee communities to test whether high‐ranking females (1) increase gregariousness and (2) minimize their travel costs. We found that high‐ranking females were more gregarious than low‐rankers only when food was scarce. During periods of food scarcity, high rank allowed females to enjoy benefits of gregariousness, while low‐ranking females strongly decreased their gregariousness. High‐ranking females traveled more than low‐ranking females, suggesting that low‐rankers might follow a strategy to minimize energy expenditure. Our results suggest that, in contrast to other chimpanzee populations and depending on the prevailing ecological conditions, female chimpanzees at Taï respond differently to varying levels of feeding competition. Care needs to be taken before generalizing results found in any one chimpanzee population to the species level. Am. J. Primatol. 73:305–313, 2011. © 2010 Wiley‐Liss, Inc.     

Sex-biased dispersal in eastern chipmunks, Tamias striatus

I investigated the effect of male mate competition and inbreeding avoidance on natal dispersal of chipmunks by longitudinally monitoring known individuals from 1986 to 1990. Natal males exhibited greater absolute and effective dispersal distances but dispersed at the same proportion as natal females. Recruitment of juvenile males was negatively affected by density of resident males, but there was no evidence of local mate competition among male kin. Analysis of the spatial distribution of neighbors showed that natal males settled farther from their mothers than did their female siblings and farther than unrelated juvenile males. In addition, mothers apparently tolerated daughters as close neighbors and occasionally shared den sites with grandprogeny. Sexually mature males were never neighbors of their mothers and were never observed at maternal mating bouts. Males may disperse to improve reproductive opportunities by avoiding competition with resident males, and by increasing access to unrelated females. Maternal tolerance of daughters but not sons may result in the close affiliation between mothers and daughters, and indirectly contribute to dispersal of natal males. Hence male-biased dispersal could be a consequence of mate competition and maternal avoidance of incestuous matings. This revised version was published online in July 2006 with corrections to the Cover Date.     

Juvenile social play and yearling behavior and reproductive success in female Belding’s ground squirrels

Benefits of play behavior have been described for individuals during the juvenile period; however, it is less clear whether benefits of juvenile play commonly extend beyond the period of juvenile development. I evaluated possible associations between juvenile social play and yearling maternal territorial behavior and reproductive success in female Belding’s ground squirrels (Urocitellus beldingi). Higher rates of juvenile social play were associated with greater intensity of territorial aggressive and vigilant behavior during gestation but not later phases of the yearling reproductive cycle, suggesting that both juvenile play and later experience may influence maternal territorial behavior in yearling females. Juvenile social play was also a reliable predictor of whether a yearling female successfully weaned a litter, raising the possibility that juvenile play behavior influences yearling reproductive success via effects on maternal territorial behavior in female U. beldingi. Other factors were also related to reproductive success in yearling females. Body mass at the beginning of the yearling reproductive period was not correlated with juvenile social play but was associated with the likelihood of successfully weaning a litter. Yearling females whose mother was still alive were more likely to wean a litter than those whose mother was not alive. Mothers and yearling daughters tended to have maternal territories near each other, and mothers with a surviving yearling daughter expressed aggressive behavior at elevated rates and directed aggression toward intruders on the daughter’s territory. Overall, results of the study suggest that juvenile social play is among the variables that influence maternal territorial behavior and reproductive success in yearling female U. beldingi, and are consistent with the idea that juvenile play has benefits beyond the juvenile period for female U. beldingi.     

The Consequences of Predation Risk on the Male Territorial Behavior in a Solitary Bee

Territorial males may adopt a mating tactic that yields greater reproductive success but that at the same time increases the risk of predation. Plasticity in reproductive behavior can reflect a balance between sexual selection and natural selection. In this study, we sought to verify the effect of predation risk on territorial behavior of males of the solitary bee Ptilothrix fructifera (Apidae). Males of the species employ alternative mating tactics and can be territorial in defense of larval food sources. By manipulating predator models in the field, we tested whether (1) males avoid perch flowers containing predator models; (2) males alternate between mating tactics when their territory is associated with a predation risk; and (3) female foraging on flowers in a territory is altered in the presence of a predator model. We measured the responses of males and females in flowers containing and not containing a model of a spider or a stuffed bird. The results show that territorial males of P. fructifera alter their territorial behavior when faced with a high risk of predation. They do not abandon their territory or change to a non‐territorial mating tactic, but instead change the use of their territory, avoiding flowers containing predator models or perching on other flowers when the previous flower presented a potential predation risk. Female P. fructifera decreases the frequency of their visits to flowers and the length of time spent there in the presence of a spider model. In short, in the face of predation risk, females and males alter their behaviors at the cost of less efficient foraging and searching for partners, respectively.     

In poor families, mothers' milk is richer for daughters than sons: A test of Trivers-Willard hypothesis in agropastoral settlements in Northern Kenya

The Trivers–Willard hypothesis predicts the unequal parental investment between daughters and sons, depending on maternal condition and offspring reproductive potential. Specifically, in polygynous populations where males have higher reproductive variance than females, it predicts that mothers in good condition will invest more in sons, whereas mothers in poor condition will invest more in daughters. Previous studies testing this hypothesis focused on behavioral investment, whereas few examined biological investment. This study investigates the Trivers–Willard hypothesis on both behavioral and biological parental investment by examining breastfeeding frequencies and breast milk fat concentrations. Data from exclusively breastfeeding mothers in Northern Kenya were used to test hypotheses: Economically sufficient mothers will breastfeed sons more frequently than daughters, whereas poor mothers will breastfeed daughters more frequently than sons, and economically sufficient mothers will produce breast milk with higher fat concentration for sons than daughters, whereas poor mothers will produce breast milk with higher fat concentration for daughters than sons. Linear regression models were applied, using breastfeeding frequency or log‐transformed milk fat as the dependent variable, and offspring's sex (son = 1/daughter = 0), socioeconomic status (higher = 1/lower = 0), and the sex‐wealth interaction as the predictors, controlling for covariates. Our results only supported the milk fat hypothesis: infant's sex and socioeconomic status interacted (P = 0.014, n = 72) in their relation with milk fat concentration. The model estimated that economically sufficient mothers produced richer milk for sons than daughters (2.8 vs. 0.6 gm/dl) while poor mothers produced richer milk for daughters than sons (2.6 vs. 2.3 gm/dl). Further research on milk constituents in relation to offspring's sex is warranted. Am J Phys Anthropol , 2012. © 2012 Wiley Periodicals, Inc.     

Weaving a tight social net: Allogrooming in free-ranging female langurs (Presbytis entellus)

We studied grooming among adults of a one-male multifemale troop of free-ranging Hanuman langurs (Presbytis entellus)living near Jodhpur, India, for 9 years. The 11–13 females devoted about 6% of their day to allogrooming. Adult males, whose tenures averaged 2.2 years, were transient figures in the troop's history, as reflected by their rather peripheral role in the grooming network. Females groomed males 4–40 times more frequently (1006 episodes) than vice versa- (176 episodes). Adult females received 97% of all grooming from other adult females (6655 episodes). Although females exhibited an age- inversed dominance hierarchy, they did not compete for grooming access to particular troop mates. Dyads of all possible rank differences occurred as frequently as expected: 51% of grooming was directed up the hierarchy and 49% down it. Young, high- ranking individuals gave and received significantly more grooming than the oldest, low- ranking females did. The pattern seemed to be influenced by kin selection because of the presumably high degree of female relatedness. They invested most in troopmates with the highest reproductive value, i.e., the youngest individuals. This trend was coupled with a preference of closest kin (mothers and daughters). Reciprocity was the outstanding feature since all adult females groomed and were groomed by all others. Such a tight social net might establish the necessary cohesion during frequent territorial disputes with neighboring troops.     

Social Relationships between Males and Females in Rock Lizard (<Emphasis Type="Italic">Darevskia brauneri</Emphasis>, Lacertidae). 2. Searching for an Area of Stable Residence,Criteria for Choice of Social Partner,and Factors of Friendly Integration of Dyads

Long-termed intersexual friendly relationships between males and females of the Brauner’s lizard are characterized by high levels of spatial association and high frequency of affiliative behavior between partners (see report 1). In present article we consider changes in the frequency of affiliative behavior in males (Am) and females (Af) after the first appearance of female on the male’s territory and conditions for the transition of lizard to stable residency (SR). Generally, Am becomes stable during the first days of initial period and does not change later. This fact suggests that in most instances male’s choice criteria are some peculiarities of the female’s exterior. In the initial period, Af is always low, however, gradually rises to the level of Am if Am is high. The main condition of female’s SR is high Am of the owner of the territory where female establishes her comfort areas. Hence, social partner choice in female is based on male’s behavior, and high Am triggers the formation of friendly interrelations. Significant correlation between social and sexual interrelations is absent. As can be judged by female’s reactions to male’s sexual behavior, his sexual activity is rather a factor of social disintegration. Structure of costs for social partner search is different in males and females, and these differences well harmonize with differences in gender strategies of partner choice. The social strategies are well interpreted in terms of the optimal foraging theory.     

Big mothers invest more in daughters – reversed sex allocation in a weakly polygynous mammal

How mothers allocate resources to offspring is central to understanding life history strategies. High quality mothers are predicted to favour investment in sons over daughters when to do so increases inclusive fitness. This is the case in ungulates with polygynous mating systems, where reproductive success is more variable among males than females, but information is scarce on sex allocation in less polygynous species. Here, for the weakly dimorphic roe deer, we show that as maternal capacity to invest increases, mothers increase allocation to daughters more than to sons, so that relative allocation to daughters increases markedly with increasing maternal quality. This cannot be explained by a between sex difference in growth priority, hence we conclude that this is evidence for active maternal discrimination. Further, we demonstrate that condition differences between offspring persist to adulthood. For high quality mothers of weakly polygynous species, daughters may be more valuable than sons.