Better few than hungry: flexible feeding ecology of collared lemurs Eulemur collaris in littoral forest fragments.

BACKGROUND: Frugivorous primates are known to encounter many problems to cope with habitat degradation, due to the fluctuating spatial and temporal distribution of their food resources. Since lemur communities evolved strategies to deal with periods of food scarcity, these primates are expected to be naturally adapted to fluctuating ecological conditions and to tolerate a certain degree of habitat changes. However, behavioral and ecological strategies adopted by frugivorous lemurs to survive in secondary habitats have been little investigated. Here, we compared the behavioral ecology of collared lemurs (Eulemur collaris) in a degraded fragment of littoral forest of south-east Madagascar, Mandena, with that of their conspecifics in a more intact habitat, Sainte Luce. METHODOLOGY/PRINCIPAL FINDINGS: Lemur groups in Mandena and in Sainte Luce were censused in 2004/2007 and in 2000, respectively. Data were collected via instantaneous sampling on five lemur groups totaling 1,698 observation hours. The Shannon index was used to determine dietary diversity and nutritional analyses were conducted to assess food quality. All feeding trees were identified and measured, and ranging areas determined via the minimum convex polygon. In the degraded area lemurs were able to modify several aspects of their feeding strategies by decreasing group size and by increasing feeding time, ranging areas, and number of feeding trees. The above strategies were apparently able to counteract a clear reduction in both food quality and size of feeding trees. CONCLUSIONS/SIGNIFICANCE: Our findings indicate that collared lemurs in littoral forest fragments modified their behavior to cope with the pressures of fluctuating resource availability. The observed flexibility is likely to be an adaptation to Malagasy rainforests, which are known to undergo periods of fruit scarcity and low productivity. These results should be carefully considered when relocating lemurs or when selecting suitable areas for their conservation.

Behavioral thermoregulation in a gregarious lemur, Eulemur collaris: effects of climatic and dietary-related factors.

Primates deal with fluctuations of the thermal environment by both physiological and behavioral mechanisms of thermoregulation. In this article we focus on non-hibernating lemurs, which are hypometabolic and have to cope with a seasonal environment. Behavioral thermoregulation has received little attention compared with specific physiological adaptations to seasonality, i.e., hibernation and torpor, which characterize a number of lemurs. We investigated the role of seasonality and dietary-related factors in determining frequencies of resting, social and postural thermoregulation, and microhabitat selection in collared lemurs, Eulemur collaris. We observed two groups of collared lemurs over a 14-month period in the littoral forest of Sainte Luce, Southern Madagascar. Frequencies of total resting and time spent in huddling, prone, and curled postures were collected via 5-min instantaneous sampling. Microhabitat selection was evaluated as the proportion of time spent in the upper canopy as compared with other layers. Climatic variables were recorded by automatic data loggers, while dietary variables were derived from phenological data and nutritional analyses of the ingested food items. We weighted the combined effects of climatic and dietary variables on the different types of behavioral thermoregulation by means of canonical correlation analysis. The model with the strongest canonical correlation included a first root representing mainly feeding time, day length, and ambient temperature and a second root representing diet quality and height of feeding trees. The output indicated that collared lemurs adapt to thermal and dietary-related metabolic stress by adjusting resting time, social, and postural thermoregulation.

Influence of abiotic factors on cathemeral activity: the case of Eulemur fulvus collaris in the littoral forest of Madagascar.

The role environmental factors play in influencing circadian rhythms in natural habitats is still poorly described in primates, especially for those taxa with an activity cycle extended over the 24-hour cycle. In this paper, we elucidate the importance of abiotic factors in entraining the activity of cathemeral primates, focussing on results from a long-term study of Eulemur fulvus collaris (collared brown lemur) in south-eastern Malagasy littoral forest. Two groups of lemurs were followed for 60 whole-day and 59 whole-night observation periods over 14 months. Diurnal and nocturnal observations were equally distributed among moon phases and seasons. Temperature and humidity were recorded hourly by automatic data loggers. The littoral forest has a climatic environment where rainfall and humidity are uncorrelated with temperature and photoperiod. Diurnal and nocturnal activity varied seasonally, with the former increasing significantly with extended day length and the latter increasing significantly with shortened day length. Dusk seemed to act as a primary zeitgeber for these lemurs, coordinating the onset of evening activity throughout the entire year. Lunar phase and the nocturnal luminosity index correlated positively with the duration of nocturnal activity and negatively with the length of diurnal activity. Temperature was positively associated with diurnal activity but did not seem to influence lemur rhythms at night. Finally, lemur nocturnal activity significantly decreased when levels of humidity and rainfall were high. Cathemeral biorhythm is triggered by zeitgebers and influenced by masking factors. The activity of collared brown lemurs appears to be seasonally influenced by photoperiod and directly modulated by nocturnal ambient luminosity. These results are discussed by comparing data from other cathemeral species living in various climatic situations.

Coexistence of melorheostosis and DISH in a female skeleton from Magna Graecia (Sixth Century BC).

This paper reports on a case of massive hyperostotic alterations observed in the skeleton of an adult woman from the necropolis of Montescaglioso Belvedere (Basilicata, Southern Italy) attributed to the Enotrian culture and dated to the 6th century BC. Hyperostotic changes involve joints, the vertebral column, and the lower limbs. In particular, the large flowing ossification in both the thoracic (T6-T10) and lumbar (L2-L5) tracts, the sacralization of L5, accompanied by sacroiliac fusion on the left side, and the proliferative bone production on both the metaphyseal portion of the left tibia and the left third metatarsal are described. The vertebral antero-lateral ossification and the sacroiliac fusion support a diagnosis of diffuse idiopathic skeletal hyperostosis (DISH), while the flowing bone formation on the lower limbs supports a diagnosis of melorheostosis. The pathological conditions described here were already described in the literature, but this is the first reported case of the coexistence of DISH and the very rare melorheostosis. Furthermore, the skeleton from Montescaglioso Belvedere represents the first case of this disease described for ancient Europe, therefore adding a valuable contribution to the reconstruction of the antiquity and distribution of skeletal dysplasias.

Dispersion dimorphism in human populations.

The aim of this paper is to verify the existence of dispersion (or variability) dimorphism in several anthropometric traits, i.e., some skeletal, muscular, and adipose dimensions, and to provide an evaluation of this scarcely considered aspect of sex differences. This research focuses on two human samples from two different European regions, Sardinia (Italy) and the Basque Country (Spain). Twenty-three anthropometric measurements were taken. A first qualitative analysis was carried out comparing the profiles of the coefficients of variation of each variable in both sexes. Secondly, the equality of variability was verified with different tests. In the normal case, Student's t-test, as proposed by Sokal and Braumann ([1980] Syst. Zool. 29:50-63), was applied. In the more general case, it was necessary to resort to resampling techniques. A suitable bootstrap test was constructed and the results were compared, when possible, with those obtained by other methods. The measurements showed parallel trends in the two populations. In particular, subcutaneous skinfolds showed significant dispersion dimorphism, with the greatest coefficients of variation in men. We suggest that this result was linked to stronger canalization in female dimensions related to the reproductive function and influenced by sociocultural factors. We also suggest defining dispersion dimorphism, whose existence is confirmed by the results presented in this paper, as a descriptive pattern of phenotype variability in both sexes that can be specific of a given class of anthropometric traits.

Differences in the endocrine and behavioral profiles during the peripartum period in macaques.

The present investigation aims to assess the changes in both social interaction and sex steroids excreted in feces of group-living Japanese macaques and rhesus monkeys. By comparing profiles of estrone conjugates (E1C) and pregnanediol-glucuronide (PdG) with the behavioral propensities of two closely related species living in similar environments, we could test the hypothesis that the social behavior of pregnant females shows significant hormonally mediated changes during the late prepartum and early postpartum period. We found a general tendency to withdraw from social life across pregnancy in both species. These behavioral changes were paralleled by endocrine profiles showing a slight prepartum increase in E1C during the last week in the rhesus group, whereas the increase was more marked and continuous in the Japanese macaque group. PdG increased slightly in rhesus macaques, whereas in Japanese macaques the fluctuations were not significant. Postpartum, both hormones dropped to low levels in both species, with no significant variation therein. Consequent to these changes, the E1C/PdG ratio increased significantly in late pregnancy only in the Japanese macaque group. Overall, these results show significant differences in the social behavior and endocrine profiles of two closely related species, thus complementing previous findings and indicating species-specific characteristics of the association between changes in affiliative behaviors and hormonal fluctuations. In particular, the shift between grooming performed and self-grooming, which showed the closest association with variations in the E1C/PdG ratio, could represent a reliable indicator of the change in the internal status of pregnant females, and is probably functional to infant survival.

Peripartum sex steroid changes and maternal style in rhesus and Japanese macaques.

The subtle and complex relationships between the sequential maturation of the endocrine systems during pregnancy and parturition, and the hormonal role in activating the central nervous system to express maternal behavior in primates, are far from being completely understood. Recent studies on the association between sex steroids and maternal behavior have yielded conflicting results in this group. Here we use a comparative approach to assess the correlation between changes in the peripartum endocrine profiles and maternal styles in two closely related macaque species, housed in analogous environments. We included in this study the first seven Japanese macaque and seven rhesus macaque mother-infant pairs born during the birth season of 2001 at the Primate Research Institute, Kyoto University, Japan. We observed each pair 3h/week (six weekly 30-min observation sessions) during the first 12 weeks of lactation. We collected fecal samples twice a week from each mother, starting 4 weeks before parturition and ending 4 weeks after parturition. We tested the hypothesis that neuroendocrine changes during pregnancy and lactation might specifically contribute to the regulation and timing of infant rejection. Despite their biological similarities, we observed a clear difference in maternal style between the two groups concerning rejection rates: rhesus macaque mothers rejected their infants earlier and more frequently throughout the whole 12 weeks of study. On the other hand, protectiveness showed similar patterns and values in the two groups, and maternal warmth was significantly higher in the rhesus group, but it followed a similar pattern over time. We also confirmed an association between maternal rejection and excreted estrogen, but not excreted progesterone, for Japanese macaques. This association was not apparent for the rhesus macaques. This result, coupled with the observation that rhesus mothers are more rejecting than Japanese macaque mothers, tends to support our hypothesis. As a group, rhesus macaques are less inhibited in the rejection of their infants, and this is paralleled by a less marked change in the primacy of estrogen in the last phase of pregnancy. On the contrary, the Japanese group is characterized by higher levels of E(1)C and the E(1)C/PdG ratio. Therefore, according to our hypothesis, their tendency to increase the rejection rate may be suppressed through a feedback loop that enhances maternal motivation and results in a more tolerant outcome toward the infant.

Mother-infant relationships and maternal estrogen metabolites changes in macaques (Macaca fuscata, M. mulatta).

This research assessed mother-infant relationships in rhesus and Japanese macaques living in analogous captive social groups, and monitored changes in the levels of excreted estrogen metabolites during the peripartum period. Each mother-infant pair was focally observed 3 h per week during the first 12 weeks of life of newborns. Fecal samples were collected twice a week from each mother, starting 4 weeks before delivery and ending 4 weeks after delivery. Infant-directed behaviors appeared to be consistently less protective/controlling and more rejecting in rhesus macaques than in Japanese macaques. Estrogen metabolite levels during the perinatal period were, on average, 3-fold higher in Japanese macaques and showed a sharp increase during the last weeks of pregnancy only in the Japanese macaque group. Considering the ecological and behavioral similarities between Japanese and rhesus macaques, the divergence between the two species in the onset and maintenance of maternal behavior was unexpected. This was possibly linked to the difference in the overall body size and life history, and to the striking divergence in estrogen metabolite variation during the peripartum period. Group size, social relationships, and average age of individuals in the two captive groups were not clearly involved in the recorded differences in maternal behavior.

Nonalimentary tooth use in prehistory: an example from early Holocene in Central Sahara (Uan Muhuggiag, Tadrart Acacus, Libya).

Signs of nonalimentary tooth use were observed on the dentition of an adult male from a single burial excavated in an area close to the Uan Muhuggiag rock shelter (Tadrart Acacus, Libya), dated to more than 7800 uncalibrated years BP, that represents the most ancient human remain found in the Libyan Sahara, and provides a first glimpse of human adaptation in the early Holocene of this region. The wear pattern shows large grooves running across the occlusal surfaces of maxillary and mandibular anterior teeth and premolars. The results of macroscopic and microscopic observation, together with scanning electron microscope (SEM) examination and experimental tests, suggest that the microdamage might be due to repeated friction of vegetal fibers, probably as a consequence of basket making, net production, or mat processing. Further data are needed to allow us to distinguish among plant-oriented activities related to food acquisition (e.g., rope and net processing), food storage (e.g., basket making), or domestic handicraft (e.g., mat processing), whose implications may generate different interpretations of sexual division of labor.

Peripartum cortisol levels and mother-infant interactions in Japanese macaques.

As evidence accumulates regarding the influence of hormones and stress-related conditions on maternal behavior, it becomes critical to better understand the relationship between physiological stress and the ability to cope with infants. Eight Japanese macaque females were observed 3 hr per week during the first 12 weeks after parturition; fecal samples were collected twice a week from each mother, starting 4 weeks before parturition and ending 4 weeks after parturition. Time spent in contact, maternal responsiveness, latency of response, and maternal rejection were measured and correlated with peripartum excreted cortisol and estradiol metabolite levels. Two indices of peripartum hormonal status were also tested against behavior: the postpartum stress index, and the postpartum cortisol/prepartum estradiol ratio (F/E). Postpartum cortisol levels showed a positive correlation with maternal rejection. The cortisol/estradiol ratio was positively correlated with rejection and latency of response, and negatively correlated with maternal responsiveness. Prepartum cortisol levels and the postpartum stress index did not correlate with any aspect of maternal behavior. Our findings suggest that hypothalamic-pituitary-adrenal (HPA) axis activity per se is not enough to predict the quality of interaction between mother and infant. Only when cortisol is high relative to estradiol could it be symptomatic of a possible negative feedback response involving stress, adrenal activity, and the ability of mothers to cope with the additional problems imposed by newborns.

Increase in tannin consumption by sifaka ( Propithecus verreauxi verreauxi) females during the birth season: a case for self-medication in prosimians?

In this study we report preliminary data on the consumption of tannin-rich plants by sifakas (Propithecus verreauxi verreauxi) living in the Kirindy forest, western Madagascar. Sifakas spent most of their time feeding on only a few plant species. The tannin intake during the period between the pregnancy and birth season was significantly higher in pregnant females or females with lactating infants than in non-reproductive females and males. These periparturient females secured a larger proportion of condensed tannins by short feeding bouts on plants not included in the group's limited preferred food species. The measured increase in tannin intake is puzzling in light of the fact that tannins are commonly known for their protein-binding properties. Since protein demands are highest in pregnant and lactating females, possible medicinal benefits of tannin ingestion are considered. Tannin consumption is associated with an increase in body weight and stimulation of milk secretion. Veterinarians administer tannins as an astringent, anti-hemorrhagic and anti-abortive. Their high potential as an alternative anthelminthic has also recently been recognized. Thus, when viewed as self-medicating behavior, controlled increase in tannin intake could have multiple prophylactic advantages for females during the periparturient period. The high selectivity in their plant choice, and the presence of unusual feeding habits by a particular group of individuals (females with infants) limited in time (birth season), suggests that an increase in tannin ingestion may be a self-medicating behavior with multiple directly adaptive benefits to female reproduction.