Comparative Analysis of the Vocal Repertoires of the Indri (Indri indri) and the Diademed Sifaka (Propithecus diadema)

International Journal of Primatology - Strepsirrhine vocalisations are extraordinarily diverse and cross-species comparisons are needed to explore how this variability evolved. We contributed to...     

Social boundaries in a Malagasy Prosimian,the Sifaka (Propithecus verreauxi)

Using focal animal samples, the social organization of sifakas was studied in two forests for 2500 hr spread over 18 months. Data were also obtained on the size and composition of groups at two other sites. The size and adult sex ratio of groups varied widely within populations, although population-wide sex ratios approached unity. During the brief annual mating season, some males mated with females belonging to other groups. The response of both male and female group members to the approach of a nongroup male appeared to depend on his identity. It is argued that while group size may be constrained by the availability of resources, group composition reflects the effects of small-sample demographic variations rather than the outcome of reproductive competition among or between males and females. Spatial boundaries of groups do not coincide with social or reproductive boundaries even within a single breeding season; further study is needed of the processes whereby relationships are established and maintained between individuals from different groups.     

Semantic Differences in Sifaka (Propithecus verreauxi) Alarm Calls: A Reflection of Genetic or Cultural Variants?

In this study, we compared the usage of alarm calls and anti‐predator strategies between a captive and a wild lemur population. The wild lemur population was studied earlier in Western Madagascar ( Fichtel & Kappeler 2002 ). The captive population was studied in outdoor enclosures of the Duke University Primate Center. Alarm calls and anti‐predator behavior were elicited by conducting experiments with both vocal and visual dummies. We scored the subjects’ immediate behavioral responses, including alarm calls, from video recordings made during the experiments. In principle, both populations have a mixed alarm call system with functionally referential alarm calls for aerial predators and general alarm calls for terrestrial and aerial predators and for situations associated with high arousal, such as group encounters. Although wild and captive sifakas exhibit the same alarm call system and use the same alarm call types, we discovered striking differences in the usage and perception of some of the alarm calls. We argue that these differences indicate either an evolutionary drift in the meaning of these calls or reflect cultural variation. The latter possibility is consistent with our understanding of the ontogeny of call usage and comprehension.     

Selectivity and Variability in the Diet of Milne-Edwards' Sifakas (Propithecus diadema edwardsi): Implications for Folivory and Seed-Eating

Propithecus diadema edwardsi combines a strategy of high selectivity for many food items with the use of more readily available and abundant foods. Selectivity is seen in relation to taxonomic affiliations of plants eaten, forest composition, and phenological patterns. Feeding time is concentrated on relatively uncommon species as indicated by high selection ratios. Annual and monthly dietary diversity is low, with food choices restricted to a relatively narrow set of species: a total of 82 and 73 plant species were eaten by the two groups of which, only 22 and 16% contributed >1% feeding time, however, these values fall with commonly reported ranges. Plant parts eaten varied widely from month to month, with overall variance in seed-eating higher than variance in young or mature leaf feeding. No correlation between percentage feeding time and food availability is significant; instead, monthly feeding patterns are better explained by the availability of particular plant species, which also supports a view of high selectivity in food choice. In contrast to selectivity for many seed, whole fruit, and new leaf sources, reliably abundant food sources appear to be leaves from lianas, epiphytes, and parasites, which were eaten in all focal months. While dramatic interannual differences in dietary composition in response to the absence of a preferred seed source highlight the interpretation of folivores as surviving food crunches by turning to readily available, poor quality resources, this strategy is not unique to folivores.     

Infanticide in Propithecus diadema edwardsi: An Evaluation of the Sexual Selection Hypothesis

Infanticide might be described as a reproductive strategy employed by anthropoid primate males when they immigrate into new groups. But infanticide has rarely been observed in wild prosimian primates. For the Malagasy lemurs this may reflect one or more of the following: strict breeding seasons; relative monomorphism in canine tooth and body size; small group sizes; male–female dominance relations; and male–female dyads within groups. We addressed the following questions: Do prosimian males commit infanticide in circumstances similar to those in which anthropoids do? and Is there any reproductive advantage for a highly seasonal breeder to commit infanticide? To help answer these questions, we describe the death of a 24-hr-old infant male Propithecus diadema edwardsi from wounds received during a fight between his mother, her adult daughter, and a newly immigrant male. Interbirth intervals between surviving offspring are 2 years for Propithecus diadema edwardsi; therefore, a male could dramatically shorten the time between reproductive windows by killing an infant. Whether this tactic would be favored by sexual selection cannot be addressed until more information has been collected on the length of interbirth interval due to infanticide relative to that of infant death by other causes; how social factors such as stability of breeding relationships affect long-term male reproductive success; how effective female counterstrategies are to prevent infanticide and/or whether they choose to mate with males that commit infanticide; and how often males that kill infants subsequently sire infants, particularly in groups that contain a resident male.     

Application of fecal steroid techniques to the reproductive endocrinology of female verreaux's Sifaka (Propithecus verreauxi)

Solid phase extraction, high performance liquid chromatography, and radioimmunoassay were used to test the validity of fecal steroid analysis for assessing ovarian function in sifaka (Propithecus verreauxi). Daily fecal samples were collected over a 4 month period from two cycling female sifaka, and single samples were collected from females during normal gestation and males while housed at the Duke University Primate Center. Tests of radioimmunoassay validity indicated that solid phase extraction and microradioimmunoassay techniques were reliable and accurate methods for quantifying ovarian steroids in sifaka feces. The progesterone (P₄) antibody specifically quantitated only P₄, while several estrogen metabolites made small contributions to immunoreactive measures of estradiol (E₂). A 1:10 dilution reduced these contributions to 3–15% of the estimated E₂ concentration. Although the spectral data suggested that E₂ was not the major metabolite present, it accounted for the majority of the immunoreactivity at normal assay dilutions. Fecal profiles of immunoreactive E₂ and P₄ in the conceptive female resembled serum profiles of other strepsirhines. E₂ and P₄ were elevated at the end of the conceptive cycle and were more markedly increased in late pregnancy in the two pregnant females. Mating behavior and indices of sexual interest were observed in conjunction with E₂ peaks, although not all peaks were accompanied by observations of sexual behavior. © 1995 Wiley-Liss, Inc.     

Scent Marking in Voles: A Reassessment of Over Marking, Counter Marking, and Self-Advertisement

We conducted a series of experiments to discern among the counter-marking, over-marking, and self-advertisement hypotheses for secondary marking in male prairie voles, Microtus ochrogaster , and meadow voles, M. pennsylvanicus . Secondary scent marks (those placed in an area that has already been marked by a conspecific) were not significantly greater than initial marks placed on clean substrate (a substrate without any previous scent marks) for either species and thus did not support a counter-marking hypothesis. Similarly, overlapping of initial scent marks with secondary marks occurred less often than expected by chance and did not support an over-marking hypothesis. Secondary marks tended to avoid overlap with scent marks previously deposited by a potential competitor. Our results suggest that secondary scent marking functions to self-advertise by maximizing individual identity and avoiding masking or blending with previous donors. Future studies on secondary marking should be designed to quantify the observed and expected frequency and placement of original and secondary marks to discern among alternative hypotheses for the adaptive significance of secondary marking.     

圈养条件下黑麂雄性标记行为与雌性化学信息存留位置的关系

化学物质被认为是哺乳动物标记行为信息传递的主要载体,而标记在鹿科动物的竞争雌性资源中具有重要的作用,因此本文重点对雄性黑麂的化学标记与雌性化学信息存留点的关系进行了行为学研究。观察发现面腺标记(利用额腺和眶下腺)是雌雄黑麂共有的化学标记行为,而行为性排尿和刨地行为(利用蹄腺)则仅为雄性具有的标记行为;躺卧不具有化学标记作用,而排粪在化学标记上的作用则难以确定。同时分析表明,雄性黑麂更倾向于在靠近雌性化学信息存留区的区域进行化学标记,且可能会因竞争压力的增大而扩大领域范围。     

Melanism in a Wild Sifaka Population: Darker Where Cold and Fragmented

International Journal of Primatology - Pigmentation is one of the most striking examples of diversity in the natural world. Specifically, primate pelage (hair/fur) pigmentation provides a substrate...     

Scent Marking by Males of the Mediterranean Fruit Fly, Ceratitis capitata (Diptera: Tephritidae)

Males of the Mediterranean fruit fly, Ceratitis capitata (medfly), defend individual leaves as mating territories. While perching, males release an air-borne pheromone (known to attract females) from everted rectal epithelium at the tip of the abdomen. Males also occasionally touch the substrate with the tip of their abdomen. The main objective of the present study was to determine whether such abdomen dipping was a form of intersexual signaling, i.e., whether this action resulted in increased female visitation to the territory. Following observations on the frequency of pheromone calling and abdomen dipping of individually marked males, I ran a standard set of experiments using leaves from four different plant species. Leaves were exposed to varying numbers of (mature) males and females, respectively, for varying durations, and female settlement was compared on exposed versus nonexposed leaves in laboratory cages. Exposing leaves to females had no, or little, influence on female distribution for any of the four plant species. Exposing leaves to males had little influence on subsequent female settlement for orange, coffee, or macadamia trees. However, leaves of the fig tree Ficus bejamina that were exposed to males were much more attractive to females than nonexposed leaves. I then conducted a series of additional tests using fig leaves and found that i) leaf exposure to immature males had no effect on female distribution, ii) leaf exposure to mature males for as little as 90 min increased leaf attractiveness to females, iii) prohibiting males direct contact with the leaf during exposure eliminated any effect on female settlement, and iv) females discriminated between exposed and nonexposed leaves even in physically complex environments (i.e., potted plants). The possible role of abdomen dipping in sexual advertisement of male medflies is discussed.     

Effect of Season and Age on the Gonadosomatic Index of Milne-Edwards' Sifakas (Propithecus diadema edwardsi) in Ranomafana National Park,Madagascar

Aiming to explain individual variation in gonadosomatic index (testicular volume per body weight), we examined the relationship between gonadosomatic index (GI), age, and season in a wild, seasonally breeding lemur—the Milne-Edwards' sifaka (Propithecus diadema edwardsi). Between 1987 and 2000, we captured and measured male lemurs from Ranomafana National Park in Madagascar 69 times. We used linear and polynomial regressions and residuals to examine the effect of season on GI and the effect of age on GI, after accounting for the effect caused by season among males of breeding age. As the breeding season approached, GI increased significantly, and all individuals measured in both the breeding and nonbreeding season had larger GI values in the breeding season. Among males of breeding age, we found no relationship between age and GI, after accounting for seasonal effects. Age, season and body weight fail to explain the variation remaining in GI. We discuss sperm competition, breeding-group composition, and the presence of parents as additional sources of variation in GI.     

Scent Marking in Female Prairie Voles: a Test of Alternative Hypotheses

We conducted three experiments with females in different stages of reproductive condition to test alternative hypotheses for the function of scent marking in female prairie voles, Microtus ochrogaster . The three reproductive categories were isolated females prior to sexual stimulation (anoestrous), sexually stimulated (oestrous) and lactating. Females in different reproductive condition were given the opportunity to scent mark clean unmarked substrate or areas that had previously been marked by adult females or adult males. The numbers of scent marks deposited by females did not differ statistically for females in different reproductive condition. However, there was a trend for anoestrous females to mark the most, oestrous females less, and lactating females the least. The lack of scent marking by lactating females might be to reduce conspicuousness to conspecifics or predators. Oestrous females tended to mark the most in the area marked previously by males, although the difference was not statistically significant.
Our results provide some support for a mate-attraction hypothesis and a territorial-defense hypothesis, but were most consistent with a self-advertisement hypothesis. Over marking was uncommon and did not differ by experiment or sex of previous donor. Our results suggest that the number and placement of scent marks by females are highly variable and function primarily to convey individual identity.     

Female Coordination of Group Travel in Wild Propithecus and Eulemur

Coordination of primate group movements by individual group members is generally categorized as leadership behavior, which entails several steps: deciding where to move next, initiating travel, and leading a group between food, water sources, and rest sites. Presumably, leaders are able to influence their daily foraging efficiency and nutritional intake, which could influence an individual's feeding ecology and long-term reproductive success. Within anthropoid species, females lead group movements in most female-bonded groups, while males lead groups in most nonfemale-bonded groups. Group leadership has not been described for social prosimians, which are typically not female-bonded. We describe group movements in two nonfemale-bonded, lemurid species living in southeastern Madagascar, Propithecus diadema edwardsi and Eulemur fulvus rufus. Although several social lemurids exhibit female dominance Eulemur fulvus rufus does not, and evidence for female dominance is equivocal in Propithecus diadema edwardsi. Given the ecological stresses that females face during reproduction, we predict that females in these two species will implement alternative behavioral strategies such as group leadership in conjunction with, or in the absence of, dominance interactions to improve access to food. We found that females in both species initiated and led group movements significantly more often than males did. In groups with multiple females, one female was primarily responsible for initiating and leading group movements. We conclude that female nutritional needs may determine ranging behavior to a large extent in these prosimian species, at least during months of gestation and lactation.     

Urine Scent Marking (USM): A Novel Test for Depressive-Like Behavior and a Predictor of Stress Resiliency in Mice

Decreased interest in pleasurable stimuli including social withdrawal and reduced libido are some of the key symptomatic criteria for major depression, and thus assays that measure social and sexual behavior in rodents may be highly appropriate for modeling depressive states. Here we present a novel approach for validating rodent models of depression by assessing male urine scent marking (USM) made in consequence to a spot of urine from a proestrous female. USM is an ethologically important form of sexual communication expressed by males to attract females. The expression of this behavior is highly sensitive and adaptive to environmental cues and social status. We hypothesized that male USM behavior offers a naturalistic measure of social motivation that can be used to evaluate hedonic behaviors relevant to the study of mood disorders. We demonstrated that 1) adult male mice displayed a strong preference for marking proestrous female urine with a high degree of specificity, 2) exposure to chronic social defeat profoundly decreased USM whereas exposure to environmental enrichment increased USM, 3) the standard antidepressant fluoxetine reversed declines in USM induced by social defeat, 4) USM behavior closely correlated with other hedonic measures, and 5) USM scores in non-stressed mice predicted behavioral outcomes after defeat exposure such that mice displaying high preference for marking female urine prior to social defeat showed behavioral resiliency after social defeat. The findings indicate that the USM test is a sensitive, validated measure of psychosocial stress effects that has high predictive value for examination of stress resiliency and vulnerability and their neurobiological substrates.     

The Equivocal Relationship Between Territoriality and Scent Marking in Wild Saddleback Tamarins (<Emphasis Type="Italic">Saguinus fuscicollis</Emphasis>)

Researchers have often assumed that scent marking serves a territorial function in callitrichines, although some controversy exists. To fulfill such a function, scent marks should 1) prevent intrusions, 2) ensure access to feeding resources, 3) enable avoidance of intergroup encounters, or 4) play an important role in the aggressive encounters between groups. We studied 13 saddleback tamarins (Saguinus fuscicollis) belonging to 3 free-ranging groups, which formed mixed-species troops with moustached tamarins (S. mystax) in the Amazonian rain forest of Peru. None of the predictions were confirmed. The tamarins used a border-marking strategy, marking more on the periphery of their territory. However, feeding trees in overlap and encounter areas received more scent marking but were still visited by neighboring groups. Intergroup encounters occurred more often than expected, and scent-marking frequency was not higher during them than when no other group was present. It appears that instead of defending a territory in the classic sense, the tamarins are optimizing signal transmission by depositing their scents where the probability of detection by neighbors is higher. Saddleback tamarins may use shared areas of their home ranges to exchange information with neighboring groups, perhaps regarding reproductive opportunities.     

Scent Marking, Sexual Behavior and Aggression in Male Gerbils: Comparative Analysis of Endocrine Control

SYNOPSIS. The aggressive, sexual, and scent marking behaviorsof male gerbils (Meriones unguiculatus) are sensitive to gonadalandrogens, but androgens are not equally important in the controlof each behavior. In this species, territorial residency, prioraggressive experience, and unidentified factors that contributeto large individual differences in aggressiveness, influencethe aggressive behavior of males at least as much as androgensdo. To the extent that androgens affect aggression between malegerbils, they act partially by altering aggressiveness and partiallyby altering production of aggression-eliciting cues. The natureof these cues is unknown. Understanding the role of androgensin aggression in this species is further complicated by theobservation that castration can either increase or decreaseaggression depending on the age at which the surgery is performed.In contrast, androgens play aprimary role in the control ofsexual behavior and scent marking. Both behaviors consistentlydecline following castration despite prior experience of themales. Both behaviors are also controlled by the medial preopticarea-anterior hypothalamus, an area of the brain often implicatedin the control of male sociosexual behaviors. It appears, though,that the sites, and possibly the mechanisms, of hormone actionunderlying scent marking and sexual behavior differ. Studyingboth behaviors in the same species, and whenever possible inthe same individuals, is proving to be a useful technique foridentifying such differences between behaviors as their sensitivityto steroids and to brain lesions.     

Birth Patterns in Wild and Captive Lion-Tailed Macaques (Macaca silenus)

During a 5-yr study of lion-tailed macaques in their natural habitat, we found that: 1) most births occurred from January to April (70%) and from September to December (19%), showing a bimodal pattern with a major and a minor birth peak; 2) the period of peaks remained the same over 5 yr; and 3) a similar pattern of birth peaks occurred both in groups in large forest complexes that had overlapping home ranges with other groups and in single groups that were isolated in forest fragments in the same region but with similar ecological conditions. The results suggest more of a birth seasonality than mere breeding synchronization in the wild lion-tailed macaques. We also analyzed data on births in captivity in European Zoos for 10 yr. We observed no seasonality or peaks in births, and the pattern was the same over the years. Data on rainfall suggest that resource availability in the wild habitat may not be uniform throughout the year; hence, ecological factors may play an important role in determination of birth patterns in the natural habitats of lion-tailed macaques.     

Ecological and Behavioral Aspects of Nest Building in Wild Bonobos (Pan paniscus)

Data on nest building behavior were collected from free ranging bonobos (Pan paniscus). Considering the physical features of both nests and trees used for nest construction, bonobos appeared to show various preferences: (1) Trees with small leaves were chosen more frequently than expected; (2) The majority of nests were constructed in trees of the middle forest layer (15 to 30 m) and at a mean height of 16 m; (3) nests built during the day were located higher than night nests and differed in the general mode of construction (number of trees involved). Comparing nests made by mature males and females it became apparent that females (4) built nests higher, (5) constructed day nests more frequently and (6) used them for a longer time than males. Comparison of data collected at different study sites indicates site-specific differences concerning selection of trees and location of nesting sites. Behavioral observations made clear that nests were not only used for rest but also for other activities like feeding, social grooming and play. Moreover, the study provided the first evidence that bonobos build nests also in order to avoid potential or imminent conflicts with other party members. Field observations indicate that these nests symbolize a taboo zone and show another facet of the social abilities of bonobos for the solution of intra group conflicts. It is suggested that this behavior derives from the spatial intolerance shown by females during the process of weaning.