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.     

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.     

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.     

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.     

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.     

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.