Evidence of genetic monogamy in the lemur Indri (Indri indri)

Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair‐living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra‐pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair‐living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra‐pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair‐living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair‐living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species.     

Isolation and characterization of 20 microsatellite marker loci from the Indri (Indri indri) genome

Twenty novel polymorphic microsatellite loci were isolated and characterized from the Indri, Indri indri, genome. Along with sequence data, this marker suite will be used in future studies to establish population structure throughout its range and to verify the proposed subspecific nomenclature. Gene diversity (0.760 and 0.783) and allelic richness (5.8 and 6.43) were estimated in the Betampona and Andasibe populations, respectively.     

Female dominance in Indri indri.

A total of 15 months were spent on field research in eastern Madagascar studying the largest extant lemur Indri indri. Social relationships were analysed according to the frequency and direction of affiliative and agonistic behaviours, and with respect to the relative tree positions and behavioural synchrony of group members. The relationship between the adult male and adult female in each group was distinguished by the subordinance of the former. Between group variation in adults' relationships are examined with respect to the function of this behaviour.     

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...     

Behavioral correlates of extra-pair copulation in Indri indri

Active pursuit of extra-pair mating has been reported for Indri indri, the socially monogamous largest living lemur. This study, conducted in a mountain rainforest in eastern Madagascar, presents the first evidence for extra-pair mating of indri and discusses the alternative mating strategy and alteration of the social, territorial, spatial, and vocal behavior of the adult female of a group of wild indris. Further studies may investigate whether extra-pair copulation is an attempt to breed with a partner of superior quality and thus lead to extra-pair paternity. If so, it could potentially play a role in maintaining genetic variability within a population.     

Diet and feeding behaviour of Indri indri in a low-altitude rain forest

The diet and feeding behaviour of Indri indri were investigated in the Betampona Reserve, eastern Madagascar, over 12 months from February 2000 to February 2001. The highly folivorous diet of this species was confirmed--feeding on foliage (leaves and petioles) accounting for 82% of feeding records. Immature leaves were the preferred dietary item, but at times of relative scarcity mature leaves, fruit, seeds, flowers and bark were substituted. The indri were observed to feed on parts from 22 plant families, 37 genera and at least 42 species. The most important plant families in the diet of Indri were Lauraceae, Clusiaceae and Myristicaceae. Most feeding at Betampona was observed at 5-20 m above the forest floor amongst small (2.1-5.0 cm), oblique/horizontal supports (0-45 degrees). The indri spent 41.4% of their active period feeding most commonly in above-branch postures. Studies such as this are important for the development of conservation management plans for this endangered species.     

The song of the Indris (Indri indri; Primates: Lemuroidea): Natural history,form, and function

The song of the largest Malagasy lemur was extensively studied in the field between 1972 and 1984. The song’s structure is described, and the role of song in the natural history of Indriis examined by relating the naturally occurring variability of different song parameters to the behavior of habituated groups and the composition of other groups in the population. The function of an Indrigroup’s song is complex, varying according to the location and identity of animals hearing it. Territorial aspects of the song are considered in detail and the nature of primate territorial vocalizations is critically discussed.     

Effects of anthropogenic disturbance on indri (Indri indri) health in Madagascar

Anthropogenic habitat disturbance impairs ecosystem health by fragmenting forested areas, introducing environmental contamination, and reducing the quality of habitat resources. The effect of this disturbance on wildlife health is of particular concern in Madagascar, one of the world's biodiversity hotspots, where anthropogenic pressures on the environment remain high. Despite the conservation importance of threatened lemur populations in Madagascar, few data exist on the effects of anthropogenic disturbance on lemur health. To examine these impacts, indri (Indri indri) populations were evaluated from two forest reserves that differ in their exposure to anthropogenic disturbance. We compared the health status of 36 indri individuals from two sites: one population from a protected, undisturbed area of lowland evergreen humid forest and the other population from a reserve exposed to frequent tourism and forest degradation. Comparison of indri health parameters between sites suggests an impact of anthropogenic disturbance, including significant differences in leukocyte count and differential, 12 serum parameters, 6 trace minerals, and a higher diversity of parasites, with a significant difference in the presence of the louse, Trichophilopterus babakotophilus. These data suggest that indri living in disturbed forests may experience physiological changes and increased susceptibility to parasitism, which may ultimately impair reproductive success and survival.     

An ethmoid exposure (os planum) in the orbit of Indri indri (Primates, Lemuriformes).

In 6 of 17 skulls of Indri indri retaining distinct sutures in the medial orbital wall, a small separate bony element intervenes between the frontal and the maxillolacrimal suture. This element is demonstrably continuous with the ethmoid on one such skull. The occurrence of an ethmoid exposure in the orbit of Indri suggests that this trait is not a simple function of orbital size and convergence. Since such an exposure is found in non-cheirogaleine lemuriforms, its distribution provides no support for the hyothesis that lorises and galagos are derived from cheirogaleines.     

Dietary and Feeding Differences Between Sympatric Propithecus diadema diadema and Indri indri

We analyzed the dietary profiles and feeding behaviors of Propithecus diadema diadema and Indri indri in a community of animals that reside in midaltitude rain forest within Madagascar's Mantadia National Park. Propithecus diadema diadema ate a diverse mixture of fruits, seeds, flowers and young leaves, while the bulk of the diet of Indri indri consisted of young leaves, which resulted in significantly higher levels of fat and water-soluble carbohydrates in foods eaten by Propithecus diadema diadema. Fiber values of items eaten are high (54% NDF) for both species, though not significantly different between them. The preference for immature foliage by Indri indri suggests that their overall intake of fiber is greater than that of Propithecus diadema diadema, which had a high proportion of non-leaf material in their diet. We propose that differences in gut morphology between the two indriids contribute to their disparate diets. Levels of secondary compounds were high in certain food items, but overall they are also not significantly different between the two indriid diets. Propithecus diadema diadema exhibited a strong preference for 2 alkaloid-containing seed species, while no food of Indri indri contained alkaloids. In addition, Propithecus diadema diadema consumed a higher diversity of plant species on a daily/yearly basis, exhibited more feeding bouts on a daily basis, and their feeding bouts (on young leaves, fruit and flowers) are significantly shorter in duration than those of Indri indri. Furthermore, Propithecus diadema diadema had twice the number of geophagic episodes of Indri indri.     

Sexually dimorphic phrase organization in the song of the indris (Indri indri)

Animal acoustic communication often takes the form of complex sequences, composed of multiple distinct acoustic units, which can vary in their degree of stereotypy. Studies of sequence variation may contribute to our understanding of the structural flexibility of primates' songs, which can provide essential ecological and behavioral information about variability at the individual, population, and specific level and provide insights into the mechanisms and drivers responsible for the evolutionary change of communicative traits. Several methods have been used for investigating different levels of structural information and sequence similarity in acoustic displays. We studied intra and interindividual variation in the song structuring of a singing primate, the indri (Indri indri), which inhabits the montane rain forests of Madagascar. Indri groups emit duets and choruses in which they combine long notes, short single units, and phrases consisting of a variable number of units (from two to six) with slightly descending frequency. Males' and females' contributions to the song differ in the temporal and frequency structure of song units and repertoire size. We calculated the similarity of phrase organization across different individual contributions using the Levenshtein distance, a logic distance that expressed the minimum cost to convert a sequence into another and can measure differences between two sequences of data. We then analyzed the degree of similarity within and between individuals and found that: (a) the phrase structure of songs varied between reproductive males and females: female structuring of the song showed a higher number of phrases if compared to males; (b) male contributions to the song were overall more similar to those of other males than were female contributions to the song of other females; (c) male contributions were more stereotyped than female contributions, which showed greater individual flexibility. The picture emerging from phrase combinatorics in the indris is in agreement with previous findings of rhythmic features and song repertoire size of the indris, which also suggested that female songs are potentially less stereotyped than those of males.     

Laterality of manual function in foraging and positional behavior in wild indri (Indri indri)

This research is based on the idea that some prosimian species are good models in which to test certain postulates of the "postural origins" theory proposed by MacNeilage and colleagues [Behavioral and Brain Sciences 10:247-303, 1987] to explain the evolution of hand preference within the order Primates. We investigated manual laterality in 16 wild indris (eight males and eight females, living in four social groups) in their habitat, the Madagascan tropical rain forest. Data were collected on two spontaneous behaviors: "branch-reach," an action that occurs during foraging, and "higher support," a posture typical of clingers and leapers. A total of seven subjects were significantly lateralized for branch-reach (two showed a right preference, and five showed a left preference). Four subjects were significantly lateralized for higher support, and all of them showed a right-hand preference. Most of the indris we studied showed no preference. Our research suggests that indri are at "level 1 of laterality" in the classification framework proposed by McGrew and Marchant [Yearbook of Physical Anthropology 40:201-232, 1997]. The data presented here are not discordant with the "postural origins" theory, as lateralized subjects are often in the direction predicted by MacNeilage and colleagues [Behavioral and Brain Sciences 10:247-303, 1987], but they are the minority.     

Feeding Ecology and Regurgitation–Reingestion Behavior of the Critically Endangered Indri indri in the Maromizaha Protected Area,Eastern Madagascar

International Journal of Primatology - Deforestation around the world is a major threat to primates. Understanding primate species’ habitat and dietary requirements is critical in creating...     

Sex Differences in the Song of <Emphasis Type="Italic">Indri indri</Emphasis>

In some primate species, males and females within a social group emit loud calls in a coordinated manner or chorus. Indri indri emits a very conspicuous loud call that elicits the loud calls of neighboring groups. Previous investigations have hypothesized that the main functions of the indri chorus are related to territorial announcement, intergroup avoidance, and group cohesion. We investigated sex differences in indri song. We recorded and analysed songs given by 10 different groups over 160 d. Overall singing duration did not vary between the sexes. However, males emitted significantly fewer but longer notes. Adult males and females of each group participated in the song with sex-specific repertoires. Females had a song repertoire of 8 note types; males shared all of their 6 notes with females. Apart from the initial roars, in all note types shared by both sexes, male notes were significantly longer than female ones, whereas variations in frequency parameters differed according to the note type. These findings suggest that indri song may provide cues to conspecifics, such as group size and sex composition, which could influence interactions between groups.     

Population and Conservation Genetics in an Endangered Lemur, <Emphasis Type="Italic">Indri indri</Emphasis>, Across Three Forest Reserves in Madagascar

Population decline and fragmentation often lead to reduced genetic diversity and population differentiation. Habitat destruction throughout Madagascar has caused population decline and extinction of many endemic species. Lemur populations, including those of the largest extant lemur, Indri indri, have been fragmented into remaining forest patches. We assessed the level of genetic diversity in indri populations in three protected reserves by genotyping a total of 43 individuals at 17 microsatellite loci. Genetic diversity in terms of heterozygosity was high in all three reserves, with no differences between reserves. Population structure and F _ST analyses revealed Analamazaotra Forest Station and the Torotorofotsy Conservation Area, which are separated by ca. 18 km to be genetically differentiated from each other with some admixture. Betampona Strict Nature Reserve, which is separated from the other reserves by ca. 130 km, exhibited clear population genetic differentiation, with no signs of admixture with the other reserves. Our genetic diversity estimates are similar to those for other Indridae in similar habitats and may reflect past rather than current population processes, given that populations have declined recently. Our results suggest that Betampona may be genetically isolated and that it is important to maintain gene flow between remaining populations to prevent loss of genetic diversity for the future conservation of Indri indri.     

Diurnal distribution of loud calls in sympatric wild indris (Indri indri) and ruffed lemurs (Varecia variegata): implications for call functions

We carried out a short study on the diurnal call distribution of two sympatric lemurs in the Réserve Naturelle Intégrale Zahamena (eastern Madagascar). Whereas indris (Indri) song bouts were clearly concentrated in the early morning hours, the roar/shriek choruses of ruffed lemurs (Varecia) exhibited a much more even distribution throughout the day. These differences in distribution pattern support earlier claims that indri song bouts are more likely to serve territorial functions, whereas ruffed lemur loud calls may serve both spacing and/or alarm call functions.     

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.     

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.     

Uniform hypothesis of cell behavior--movement, contact inhibition of movement, adhesion, chemotaxis, phagocytosis, pinocytosis, division, contact inhibition of division, fusion.

The cell has been represented as a charged liquid drop. Contrary to the DLVO-theory, the effect of the surface potential upon the value of the interfacial tension of the cell membrane has also been taken into consideration. The cell membrane has visco-elastic properties and its constituents may move against each other. Cell movement is caused by the appearance of a small number of the electrically charged constituents of the cell membrane on the leading edge of the cell. This produces a local decrease in the surface tension and the cell membrane expansion. At the moment of contact between two cells proton transfers occur between the strongly negatively charged microvilli of one cell and the body of the other, analogous to a condenser breakdown. This, through the effect on the surface tension, causes contact inhibition of movement. The distribution of the proton dissociable groups modifies the interaction between the cells (differentiation) and between the cell and the substratum (adhesion). Adsorption of the charged compounds at the surface of the cell membrane, decreasing the surface potential and increasing the surface tension, causes the phenomena of chemotaxis, phagocytosis and pinocytosis. Cell division, considered in the terms of the surface energy, requires an adequate supply of considerable quantities of energy inversely proportional to the surface potential value. In case of a reduction of the distance between the cells, their surface potential and the energetic barrier of the cell division processes increases, and causes contact inhibition of cell division. Due to their high charge, division of neoplastic cells is inhibited much later than division of normal cells, or is completely ininhibited due to geometric conditions. Fusion of the cell membrane in the intra-cellular and intercellular processes is a reverse process in relation to the cell division.     

Application of electroporation for transfer of plasmid DNA to Lactobacillus, Lactococcus, Leuconostoc, Listeria, Pediococcus, Bacillus, Staphylococcus, Enterococcus and Propionibacterium

Plasmid DNA was introduced by electroporation into Bacillus, Enterococcus, Lactobacillus, Lactococcus, Leuconostoc, Listeria, Pediococcus, Propionibacterium and Staphylococcus as an alternative to competent-cell or protoplast transformation. Plasmid-containing transformants were recovered in these recipients at frequencies ranging from 10(1) to 10(5) transformants micrograms-1 of pGK12. Several parameters of the protocol, including DNA concentration, voltage, plating regimen and electroporation buffers were evaluated to determine conditions that improved transformation frequencies for Lactobacillus acidophilus. Using optimized conditions, the following plasmids were introduced into L. acidophilus: pAMB1, pC194, pGB354, pGKV1, pSA3, pTRK13, pTV1 and pVA797. The ability to transfer plasmid DNA via eletroporation will greatly facilitate the application of recombinant DNA methodology and transposon technology to Gram-positive bacteria for cloning and analysis of significant genes.