Chromosomal evolution in Malagasy lemurs: X. chromosomal banding studies of Propithecus diadema edwardsi and Indri indri and phylogenic relationships between all the species of the Indriidae

The R-banded karyotypes of two Indriidae, Propithecus diadema and Indri indri, are described and compared with each other and with those of the other species of this family, previously reported, Avahi laniger and Propithecus verreauxi. These comparisons show that 30 chromosomal rearrangements, including 21 Robertsonian translocations and eight pericentric inversions, differentiate these karyotypes. A phylogenic diagram is proposed, showing the early separation of Avahi and the relatively late divergence of the three other species. A populational evolution has occurred between the three other species, but Indri is clearly separated from the two other species by at least five complex rearrangements, although it shares four Robertsonian translocations with P. verreauxi but not P. diadema.     

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.     

The diet and feeding behavior of the silver leaf monkey (Trachypithecus auratus sondaicus) in Indonesia

I describe the diet and feeding behavior of silver leaf monkeys (Trachypithecus auratus sondaicus) in the Pangandaran Nature Reserve, West Java, Indonesia, and compare a group living in old secondary rain forest with a group living in mixed plantation/secondary forest to determine intraspecific variation in feeding behavior and the importance of the plantation species in the diet of the monkeys. Young leaves and leaf buds made up slightly less than half of their diets, with both groups showing a preference for a few species when seasonally available. Fruits and flowers of a few species were also preferentially selected when available. These included sweet, fleshy fruits, which most other colobines tend to avoid. Young leaf intake was greatest in months when fruit intake was low. Mature leaves were rarely eaten. Both groups spent approximately 20% of feeding time foraging on Moraceae species. Differences in the diet of the two groups were related largely to differences in vegetational composition and the availability and abundance of food items for the species common to both sites. Teak (Tectona grandis) was the top food species of the group living in mixed plantation/secondary forest, with the midribs of young leaves preferentially selected. Young leaves ofT. grandis, available throughout the study, provided a staple food and were eaten when preferred foods were scarce. More favored food items were available to the group living in old secondary forest, though none was a staple food.     

Infant development and parental care in two species of sifakas

This paper reports the results of a three-month field study on parental care and infant development in the diademed sifaka (Propithecus diadema edwardsi) in the primary rain-forest of south-eastern Madagascar. They are compared with a three-and-a-half-month study of captive white sifaka (Propithecus verreauxi coquereli) in the Duke University Primate Centre. Records were taken by means of focal animal and instantaneous sampling. In both species the mother was the primary carrier and caretaker; theP. verreauxi father carried the infant significantly more than did any animal other than the mother in theP. diadema group. The infantP. verreauxi spent less time off the mother than didP. diadema from week 4 through week 10. It is concluded thatP. verreauxi shows more non-maternal care thanP. diadema and also develops at a slower rate. The difference in the two species' habitats is discussed as a possible cause.     

Craniodental Characters in the Taxonomy of Propithecus

The indriid genus Propithecus comprises the sifakas, medium-sized lemurs endemic to the forests of Madagascar. Traditionally, scientists divided the genus into only 2 or 3 species —Propithecus diadema, P. verreauxi, and, since 1988, P. tattersalli— with 4 or 5 subspecies in each of the first 2 taxa, but recent authors have suggested that many more distinct species should be recognized. We draw from quantitative and qualitative studies of craniodental traits to evaluate further the phenetic distinctiveness and taxonomic status of each named form of Propithecus. We recognize 9–10 species in the genus. The 4 or 5 species of the Propithecus diadema group —P. diadema, P. candidus, P. perrieri, P. edwardsi, and perhaps P. holomelas, if distinct— share several derived features, including large average body size and a mandible specialized for rotational chewing, and clearly comprise a closely related complex. The 5 species of the Propithecus verreauxi group —P. verreauxi, P. coquereli, P. deckenii, P. coronatus, P. tattersalli— are each highly distinctive morphologically and likely do not comprise a monophyletic group. In particular, we point out the highly distinctive cranial features of Propithecus coronatus, which researchers have traditionally largely overlooked.     

Population Density and Home Range Size of <Emphasis Type="Italic">Indri indri</Emphasis> in a Protected Low Altitude Rain Forest

We report the results of a census of Indri indri conducted in Betampona Nature Reserve, a lowland rain forest in eastern Madagascar. In addition, we conducted a year-long study of the ranging behavior of 3 groups in the southwestern region of the reserve. We used 2 methods to calculate population density and home range size, and to provide minimum and maximum estimates. Population density of Indri indri ranged from 6.9–13.2 individuals/km² in Betampona. Mean home range size is 27 ha. The values for population density and home range size are intermediate between values for Indri indri in selectively logged and undisturbed montane rain forest. Our results suggest a relationship between habitat disturbance, population density and home range size for the species. Recent increases in habitat disturbance appear to cause an increase in population density and a decrease in home range size. The results are consistent with ones for other folivorous primate populations. Further research on habitat requirements of Indri and availability in Betampona is necessary to investigate the possibility of translocating Indri from nearby forest fragments into Betampona.     

Ecological Correlates to Lemur Community Structure in Southeast Madagascar

The Fandriana-Marolambo forest corridor is one of the largest (ca. 250,000 ha) and least explored tracts of unprotected forest in southeast Madagascar. Although published range maps show continuous distributions for many lemurs throughout the region, there are few data on lemur community structure in the corridor. We aimed to determine lemur community structure, with its ecological correlates (altitude, agriculture, selective logging, and hunting), in the Fandriana-Marolambo forest corridor. We surveyed 7 sites and sighted 4 nocturnal taxa (Avahi laniger, Cheirogaleus major, Lepilemur mustelinus, and Microcebus rufus) and 6 diurnal taxa (Eulemur rubriventer, E. fulvus rufus, E. f. fulvus, Propithecus diadema edwardsi, Hapalemur griseus griseus, and Varecia variegata variegata). Composition of the lemur community was broadly similar to that of nearby protected areas (Ranomafana and Mantadia National Parks). However, we sighted no Hapalemur aureus, H. simus, or Indri indri, and observed Propithecus diadema edwardsi and Varecia variegata variegata at only 1 site each. We sighted an apparent hybrid form of Eulemur fulvus fulvus and E. f. rufus that may represent a new hybrid zone for lemurs. After testing for spatial autocorrelation, lemur diversity correlates negatively with altitude and agricultural intensity. Though the Government of Madagascar is assessing the corridor as a new national park, we suggest conservation plans for local lemurs are complicated by population isolation and lack of data on minimum viable size of the proposed protected area.     

Cranial and mandibular morphology of the Indrinae. Contribution of Procrustes methods and Fourier analysis

Although it is universally accepted that the Indridae family is monophyletic, there is no such unanimity about how the extant species of the Indrinae sub-family are related. Cranium and mandible disparity among Indri indri, Propithecus diadema, Propithecus verreauxi and Avahi laniger is analysed by geometrical morphometric methods and interpreted in adaptive terms. We compare results obtained by two techniques: Procrustes superimpositions for skulls and elliptical Fourier analysis for jawbones. In both studies, the three genera are clearly isolated. Avahi laniger is the species with the most paedomorphic cranium while Indri indri has the most 'juvenile' mandible. Cranial morphology is governed principally by orbit volume and body size, while jaw shape is related to diet (enlargement of the gonial region).     

Seasonal variation in positional behavior of malagasy lemurs

I describe the positional behavior of four species of Malagasy lemur (Propithecus diadema, Eulemur fulvus rufus, Eulemur rubriventer,and Varecia variegata)at two times of year at Ranomafana National Park,Madagascar. There were significant seasonal differences in locomotor behavior in all species except P. diademaAmong the lemurids, leaping was more frequent and quadrupedism less frequent in the dry season. Only E. rubriventerexhibited seasonal differences in posture, and there were few seasonal differences in support use. The observed differences in positional behavior were not the result of differences in activity budget or in microhabitat use attributable to seasonal variation in resource use.     

Chromosome Painting Technique Contributes to Constructions of Evolutionary Trees of Lemurs

We used human-specific probes for chromosomes 3, 11, 14, 15, 17, 19, 21 to paint chromosomes of four species of Indridae (Avahi laniger, Indri indri, Propithecus verreauxi, and P. diadema). All human chromosome probes hybridized specifically to chromosome segments or to whole arms of indrid chromosomes. In general, the results obtained by chromosome painting confirm those obtained by R-banding except for some reciprocal translocations undetected by R-banding. Our findings confirm that in the evolution of the Indridae, Avahi laniger first emerges, then Indri and Propithecus share a common trunk. After populational evolution, this sister clade diverged.     

Diet of the Indochinese silvered langur (Trachypithecus germaini) in Kien Luong Karst area,Kien Giang Province

The Indochinese silvered langur (Trachypithecus germaini) is distributed to the west of Mekong River in Cambodia, Lao PDR, Thailand and Vietnam. During a two‐year study, from May 2014 to May 2016, we collected 320.44 hr of behavior, with 17,040 feeding bouts recorded (142 hr) for T. germaini on Chua Hang Karst Mountain, Kien Luong District, Kien Giang Province, Vietnam. Feeding accounted for 45% of the Indochinese silvered langurs’ activity budget. The plant diet of the Indochinese silvered langurs was principally composed of young leaves (58%), followed by mature leaves (9.5%), fruits (22.7%), flowers (4.7%), buds (3.3%), petioles (1.2%), and other (0.5%). A total of 58 plant species were fed on by the silvered langurs, and leaves of eight species (Phyllathus reticulatus, Ficus rumphii, Ficus tinctoria, Ficus microcarpa, Cayratia trifolia, Streblus ilicifolia, Combretum latifolium, and Streblus asper) were fed on throughout the year. P. reticulatus was most frequently eaten (13.9% feeding time, n = 1,733). Food selection differed significantly between months and seasons. The Indochinese silvered langurs ate 27 plant species in the wet season compared with 23 plant species in the dry season. Leaf chemical composition of two food categories, 16 eaten species (with 10 most frequently consumed species and six least consumed species), and four noneaten species, were analyzed. Feeding samples from eaten species in the Indochinese silvered langurs's diet contained lower amounts of condensed tannin, lignin, protein, ash, and lipids, but a higher amount of total sugar compared with samples from noneaten species. Furthermore, the most frequently consumed species contained lower amounts of lignin compared with the less frequently consumed species. Using a generalized linear model with five variables, including neutral detergent fiber (NDF), total sugar, lignin, lipid, and calcium (Ca) indicated that NDF positively correlated and lignin content negatively correlated with feeding records in the diet of these langur.     

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.     

Nutritional correlates of the “lean season”: Effects of seasonality and frugivory on the nutritional ecology of diademed sifakas

Primate field studies often identify “lean seasons,” when preferred foods are scarce, and lower‐quality, abundant foods (fallback foods) are consumed. Here, we quantify the nutritional implications of these terms for two diademed sifaka groups (Propithecus diadema) in Madagascar, using detailed feeding observations and chemical analyses of foods. In particular, we sought to understand 1) how macronutrient and energy intakes vary seasonally, including whether these intakes respond in similar or divergent ways; 2) how the amount of food ingested varies seasonally (including whether changes in amount eaten may compensate for altered food quality); and 3) correlations between these variables and the degree of frugivory. In the lean season, sifakas shifted to non‐fruit foods (leaves and flowers), which tended to be high in protein while low in other macronutrients and energy, but the average composition of the most used foods in each season was similar. They also showed dramatic decreases in feeding time, food ingested, and consequently, daily intake of macronutrients and energy. The degree of frugivory in the daily diet was a strong positive predictor of feeding time, amount ingested and all macronutrient and energy intakes, though season had an independent effect. These results suggest that factors restricting how much food can be eaten (e.g., handling time, availability, or intrinsic characteristics like fiber and plant secondary metabolites) can be more important than the nutritional composition of foods themselves in determining nutritional outcomes—a finding with relevance for understanding seasonal changes in behavior, life history strategies, competitive regimes, and conservation planning. Am J Phys Anthropol 153:78–91, 2014. © 2013 Wiley Periodicals, Inc.     

Folivory by a tropical tanager: species of plants used and the relationship between leaf consumption and fruit abundance

ABSTRACT Folivory, or eating leaves, is unusual for small passerines. Puerto Rican Spindalises (Spindalis portoricensis, Thraupidae), tanagers endemic to the island of Puerto Rico, are known to feed on leaves, but little is known about the possible importance of leaves in their diet. Our objectives were to determine the different species of leaves eaten, the percentage of their diet consisting of leaves, and the relationship between leaf consumption and fruit abundance. We used data from previous studies where the foraging activity of Puerto Rican Spindalises was systematically sampled, and from additional observations made throughout the island. We documented 160 records of folivory, with spindalises feeding on 44 plant species in 25 plant families, including monocots, dicots, gymnosperms, and pteridophytes. Spindalises fed on young leaves of 26 plant species, and mature leaves of 19 plant species. Spindalises were primarly frugivorous (83.9% of diet), but leaves were the second most frequent food item in their diets (8.9% of diet). We also found that leaf consumption was negatively correlated with the abundance of ripe fruit, suggesting that leaves were particularly important food items when less fruit was available. The frequency of folivory by spindalises in our study was less than reported for other folivorous passerines such as plantcutters (Phytotoma spp.) and saltators (Saltator spp.). Nonetheless, folivory may help spindalises cope with human‐dominated landscapes and other environmental changes on small islands.     

Diet and feeding patterns in the kipunji (<Emphasis Type="Italic">Rungwecebus kipunji</Emphasis>) in Tanzania’s Southern Highlands: a first analysis

The diet and feeding behaviour of the kipunji (Rungwecebus kipunji) was studied over 45 months, the first dietary analysis for this species. During 9498 h of direct observation of 34 kipunji groups, a list of 122 identified foodplants was recorded. The list represents 60 families, including 64 trees, 30 herbs, 9 climbers, 7 shrubs, 6 lianas, 3 grasses and 3 ferns. Kipunji were observed eating bark, young and mature leaves, ripe and unripe fruits, flowers, pith, seed pods, rhizomes, tubers, shoots and stalks. Invertebrates, fungi, moss, lichen, and soil were also eaten. Macaranga capensis var. capensis, an early successional tree, was the most commonly consumed species, with leaves, leaf stalks, pith, flowers and bark all eaten. We demonstrate that the kipunji is an omnivorous dietary generalist, favouring mature and immature leaves, ripe and unripe fruits and bark in similar proportions, with an almost comparable fondness for leaf stalks and flowers. Kipunji appear to be adaptable foragers able to modify their diet seasonally, being more folivorous in the dry season and more frugivorous in the wet. Whereas more ripe fruit is eaten in the wet season, the proportion of unripe fruit remains similar across the year. The proportion of mature leaves and pith increases throughout the dry season at the expense of ripe fruits and bark, and this may compensate nutritionally for the lack of available dry-season ripe fruits. Relatively more pith is eaten in the dry season, more stalks at the end of the dry and beginning of the wet seasons, and bark consumption increases as the rainfall rises.     

Dietary patterns in Perrier's sifakas (Propithecus diadema perrieri): a preliminary study

Some lemur species range into only one habitat type, whereas others range into a variety of habitats. Because plant community structure can differ between habitats, dietary patterns may vary for conspecific groups of primates that range into more than one type of habitat. The goal of our study was to determine how habitat variation influences dietary patterns in Perrier's sifakas (Propithecus diadema perrieri) that range into both dry and riparian forests in northern Madagascar. We collected 542 hr of data on the behavior and diet of two groups of P.d. perrieri from 7 June to 4 August 1998 at Camp Antobiratsy in Analamera Special Reserve, Madagascar. We computed indices of dietary diversity for each group and dietary/plant species similarity between groups. P.d. perrieri in group 1 fed predominantly in dry forest (72.7% of feeding records, n=660), whereas those in group 2 fed most often in riparian forest (73.7% of feeding records, n=666). The index of dietary similarity (0.986) was significantly higher than the index of plant species similarity (0.767). Although the P.d. perrieri in the two study groups fed predominantly in different forest habitats, they ate similar food items in very comparable proportions (but not from the same plant species). However, based on habitat availability measures, neither group fed where they were expected to feed.     

Similarities,differences, and seasonal patterns in the diets ofEulemur rubriventer andEulemur fulvus rufus in the Ranomafana National Park,Madagascar

I studied the diets of two sympatric species ofEulemur (E. fulvus rufus andE. rubriventer) in the Ranomafana National Part in southeastern Madagascar from July 1988 through August 1989. Both species were highly frugivorous throughout the year and devoted similar amounts of time to feeding daily; the composition of their diets were similar. Three aspects of both lemur species' diets were correlated with seasonal food availability: changes in interspecific dietary overlap, the length of feeding bouts, and the amount of time devoted to feeding daily. Throughout the year neither species had a more diverse or more folivorous diet than its sympatric congener. However, there were several consistent year-round differences between their diets.E. f. rufus initiated more feeding bouts daily that were shorter in duration than those ofE. rubriventer. E. f. rufus also consistently exploited more unripe fruits and mature leaves thanE. rubriventer did throughout the study.E. f. rufus migrated from the study site during a period of fruit scarcity. These dietary patterns are discussed here in regard to feeding patterns observed in other sympatric congeneric primate species, whether these dietary differences can contribute to these two species' ability to coexist, and how differences in diet may be influenced by differences in social structure. I suggest that subtle, consistent differences in diet and seasonal dietary differences are sufficient to allow these two species to coexist.     

Feeding Ecology of <Emphasis Type="Italic">Trachypithecus pileatus</Emphasis> in India

We observed a group of capped langurs for 12 mo in the Pakhui Wildlife Sanctuary, Arunachal Pradesh, India. We recorded the time of feeding on different food plant species, food categories, and the feeding heights of monkeys in trees. Capped langurs spent 68% of their feeding time on leaves, 16% on flowers, and 16% on fruits. Feeding on leaves was consistently high (p < 0.01) during the year, with the highest feeding in May (85%) and the lowest in January (47%). The seasonal difference in feeding on leaves is significant (p < 0.05): it was higher in summer and during monsoon. The feeding time on flowers was maximal (35%) in March and that on fruits and seeds was minimal (38%) in January. Langurs ate 52 plant species throughout the year. The largest number of plants (6) were species of Moraceae, and langurs spent more feeding time (20%) on them alone. The number of plants eaten per month varied significantly (p < 0.05). Langurs ate Gmelina arborea, Albizzia lucida, Ficus glomereta, and Makania micrantha throughout the year. They spent 44% of their feeding time in terminal canopies and their average feeding height was 30–35 m. This is the first study to examine the feeding ecology of capped langurs and provides baseline data for the species.