Modified subfossil aye-aye incisors from southwestern Madagascar: species allocation and paleoecological significance

Two of the three drilled aye-aye incisors collected in 1901 by Grandidier at the subfossil site of Lamboharana were recently rediscovered in uncatalogued collections of the Institut de Paléontologie in Paris. These teeth are not much wider or thicker than those of the extant aye-aye (Daubentonia madagascariensis), but their arc of curvature is noticeably greater. These facts indicate that the teeth probably belong to D. robusta, a large extinct aye-aye whose dentition is otherwise unknown. No other remains referable to Daubentonia have been reported from Lamboharana, although D. robusta is known from other localities in the southwest. The presence of Daubentonia in southern Madagascar does not demonstrate that this region was markedly more humid or densely forested in the recent past. It remains to be established whether the extinction of D. robusta throughout its range in southern Madagascar, and local disappearance of D. madagascariensis everywhere but in the eastern forest biotope, is due to late Holocene climatic change, to anthropogenic effects, or both factors combined.     

The aye-aye (Daubentonia madagascariensis) found in the eastern rainforest of Madagascar

In the course of a study on the ecology of nocturnal lemurs several aye-aye (Daubentonia madagascariensis) were seen in the eastern rainforest of Madagascar near Perinet. These observations of the aye-aye in a forest of higher altitude suggest a still much wider distribution of this species than previously thought.     

Hand and body position during locomotor behavior in the aye-aye (Daubentonia madagascariensis)

Aye-ayes (Daubentonia madagascariensis) have unique hands among primates, with extraordinarily long fingers in relation to body size. These long digits may be vulnerable to damage from forces during locomotion, particularly during head-first descent-a locomotor mode that the aye-aye utilizes frequently. Previous behavioral studies of aye-aye locomotion reported that Daubentonia must curl its fingers during horizontal quadrupedalism and/or descent to reduce potential stresses on its long fingers. To test this hypothesis, we examined hand and body position in three captive adult aye-ayes while they walked quadrupedally on horizontal and oblique branches. Substantial variation in hand position was observed among individuals for each substrate orientation. While hand postures with curled fingers were preferred by one individual during descent, they were not preferred by the other two individuals, contrary to our expectations. Differences in body position were more consistent among all three individuals. The angle of the body relative to the substrate was significantly reduced during descent (8.4 degrees ) compared to horizontal locomotion (16.9 degrees ). These results suggest that changes in body position, rather than hand position, may help reduce stresses on the digits. A biomechanical model is proposed that demonstrates how a reduction in the body angle in relation to substrate may act to move the center of mass more caudally. This mechanism of moderating loads by altering body position, rather than hand position, may represent an important functional aspect of arboreal locomotion in aye-ayes and other primates.     

Specialized use of two fingers in free-ranging aye-ayes (Daubentonia madagascariensis)

The aye-aye (Daubentonia madagascariensis) possesses a highly specialized hand with two fingers, the third and the fourth, being used in a way unparalleled by any other primate. We observed the use of the third and the fourth fingers in various activities in four free-ranging aye-ayes. We found that the thin third finger was used exclusively or preferably for tapping, inserting into the mouth (probably for cleaning the teeth) and probing for nectar, kernels and insects in bamboo, twigs and live wood. In contrast, the robust fourth finger was used preferably when eating jackfruit (Artocarpus heterophyllus). When probing for invertebrates in soft plant tissues and in dead wood, both fingers were used in high proportions. To extract the contents from coconuts, the two fingers were apparently used for different tasks. From this small (686 observations), but unique, study of free-ranging aye-ayes, we conclude that the third finger appears to be specialized for use in tasks requiring high mobility, sensitivity and precision, whereas the fourth finger appears to be specialized for tasks requiring strength, scooping action and deep access.     

Characterization of chromosomes and localization of the rDNA locus in the aye-aye (Daubentonia madagascariensis).

The karyotype of a prosimian primate, the aye-aye (Daubentonia madagascariensis), is described. Results from a variety of staining methods (Q-, R-, G-, and C-banding, distamycin A/DAPI and methyl-green/DAPI) are reported. Sites of methylation were visualized using antibodies against 5-methylcytosine. Digestion of aye-aye fixed metaphase chromosomes with the restriction endonuclease HaeIII produced G-banding. No other restriction enzymes tested produced clear G- or C-banding patterns. Ag-staining of the nucleolar organizer regions (NORs) revealed the location of rDNA sites on the short arms of the smallest pairs of acrocentric chromosomes, 13p and 14p.     

An endogenous foamy virus in the aye-aye (Daubentonia madagascariensis)

We report the discovery and analysis of an endogenous foamy virus (PSFVaye) within the genome of the aye-aye (Daubentonia madagascariensis), a strepsirrhine primate from Madagascar. Phylogenetic analyses indicate that PSFVaye is divergent from all known simian foamy viruses, suggesting an association between foamy viruses and primates since the haplorrhine-strepsirrhine split. The discovery of PSFVaye indicates that primate foamy virus might be more broadly distributed than previously thought.     

Deadwood Structural Properties May Influence Aye-Aye (<Emphasis Type="Italic">Daubentonia madagascariensis</Emphasis>) Extractive Foraging Behavior

The identification of critical, limited natural resources for different primate species is important for advancing our understanding of behavioral ecology and toward future conservation efforts. The aye-aye (Daubentonia madagascariensis) is an Endangered nocturnal lemur with adaptations for accessing structurally defended foods: continuously growing incisors; an elongated, flexible middle finger; and a specialized auditory system. In some seasons, ca. 90% of the aye-aye’s diet consists of two structurally defended resources: 1) the larvae of wood boring insects, extracted after the aye-aye gnaws through decomposing bark (deadwood), and 2) the seeds of Canarium trees. Aye-ayes have very large individual home ranges relative to most other lemurs, possibly owing to limited resource availability. Identification of limiting dietary factor(s) is critical for our understanding of aye-aye behavioral ecology and future conservation efforts. To investigate whether aye-ayes equally access all deadwood resources within their range, we surveyed two 100 × 100 m forest plots within the territories of two aye-ayes at Sangasanga, Kianjavato, Madagascar. Only 2 of 150 deadwood specimens within the plots (1.3%) appeared to have been accessed by the aye-ayes. To test whether any external or internal deadwood properties explain aye-aye foraging preferences we recorded species, height and diameter, and quantified the internal tree density using a 3D acoustic tomograph for each foraged and nonforaged deadwood resource within the plots, plus 13 specimens (5 foraged and 8 nonforaged) outside the plots. We did not detect any statistically significant preferences for species, diameter, or height. However, results from the acoustic analysis tentatively indicated that aye-ayes are more likely to forage in trees with greater internal (≥6 cm from the bark) densities. This interior region may function as a sounding board in the tap-foraging process to help aye-ayes accurately identify potential grub-containing cavities in the outer 1–4 cm of deadwood.     

Percussive Foraging: Stimuli for Prey Location by Aye-Ayes (Daubentonia madagascariensis)

Aye-ayes (Daubentonia madagascariensis) use the thin middle finger to tap on wood in search of subsurface cavities containing insect larvae. When a cavity is located, they gnaw away wood until the prey can be extracted. Previous researchers suggested that acoustical cues reveal cavity location. We designed five studies to identify the cavity features that provide acoustical cues. When cavities were backfilled with gelatin or acoustical foam, excavation was still successful, suggesting that the reverberation of sound in air-filled cavities is not necessary for detection. Moreover, when the density of cavity content was varied, there was no difference in excavation frequency. On the other hand, a one-dimensional break in the subsurface wood was an effective stimulus for excavation. These studies suggest that a simple interface beneath the surface is sufficient to elicit excavation and that neither prey nor cavity nor even small air pockets are necessary to elicit the behavior. These results raise provocative questions as to how the aye-aye manages to forage efficiently.     

Structural characterization of neutral and acidic oligosaccharides in the milks of strepsirrhine primates: greater galago, aye-aye, Coquerel’s sifaka and mongoose lemur

The structures of milk oligosaccharides were characterized for four strepsirrhine primates to examine the extent to which they resemble milk oligosaccharides in other primates. Neutral and acidic oligosaccharides were isolated from milk of the greater galago (Galagidae: Otolemur crassicaudatus), aye-aye (Daubentoniidae: Daubentonia madagascariensis), Coquerel's sifaka (Indriidae: Propithecus coquereli) and mongoose lemur (Lemuridae: Eulemur mongoz), and their chemical structures were characterized by (1)H-NMR spectroscopy. The oligosaccharide patterns observed among strepsirrhines did not appear to correlate to phylogeny, sociality or pattern of infant care. Both type I and type II neutral oligosaccharides were found in the milk of the aye-aye, but type II predominate over type I. Only type II oligosaccharides were identified in other strepsirrhine milks. α3'-GL (isoglobotriose, Gal(α1-3)Gal(β1-4)Glc) was found in the milks of Coquerel's sifaka and mongoose lemur, which is the first report of this oligosaccharide in the milk of any primate species. 2'-FL (Fuc(α1-2)Gal(β1-4)Glc) was found in the milk of an aye-aye with an ill infant. Oligosaccharides containing the Lewis x epitope were found in aye-aye and mongoose lemur milk. Among acidic oligosaccharides, 3'-N-acetylneuraminyllactose (3'-SL-NAc, Neu5Ac(α2-3)Gal(β1-4)Glc) was found in all studied species, whereas 6'-N-acetylneuraminyllactose (6'-SL-NAc, Neu5Ac(α2-6)Gal(β1-4)Glc) was found in all species except greater galago. Greater galago milk also contained 3'-N-glycolylneuraminyllactose (3'-SL-NGc, Neu5Gc(α2-3)Gal(β1-4)Glc). The finding of a variety of neutral and acidic oligosaccharides in the milks of strepsirrhines, as previously reported for haplorhines, suggests that such constituents are ancient rather than derived features, and are as characteristic of primate lactation is the classic disaccharide, lactose.     

Signatures of functional constraint at aye-aye opsin genes: the potential of adaptive color vision in a nocturnal primate

While color vision perception is thought to be adaptively correlated with foraging efficiency for diurnal mammals, those that forage exclusively at night may not need color vision nor have the capacity for it. Indeed, although the basic condition for mammals is dichromacy, diverse nocturnal mammals have only monochromatic vision, resulting from functional loss of the short-wavelength sensitive opsin gene. However, many nocturnal primates maintain intact two opsin genes and thus have dichromatic capacity. The evolutionary significance of this surprising observation has not yet been elucidated. We used a molecular population genetics approach to test evolutionary hypotheses for the two intact opsin genes of the fully nocturnal aye-aye (Daubentonia madagascariensis), a highly unusual and endangered Madagascar primate. No evidence of gene degradation in either opsin gene was observed for any of 8 aye-aye individuals examined. Furthermore, levels of nucleotide diversity for opsin gene functional sites were lower than those for 15 neutrally evolving intergenic regions (>25 kb in total), which is consistent with a history of purifying selection on aye-aye opsin genes. The most likely explanation for these findings is that dichromacy is advantageous for aye-ayes despite their nocturnal activity pattern. We speculate that dichromatic nocturnal primates may be able to perceive color while foraging under moonlight conditions, and suggest that behavioral and ecological comparisons among dichromatic and monochromatic nocturnal primates will help to elucidate the specific activities for which color vision perception is advantageous.     

Feeding sites for extractive foraging by the aye-aye,Daubentonia madagascariensis

The aye-aye, Daubentonia madagascariensis, uses its middle digit to tap on woody sources in search of subsurface cavities containing prey. The acoustical properties of these cavities are thought to be important to this percussive foraging, but the contributions of cavity size, configuration, and contents to efficient prey capture are not known. The purpose of this study was to characterize these cavities and their residents. An analysis of foraged trees at two sites in Madagascar revealed that many of the foraged cavities are mines bored by large cerambycid beetle larvae. Apparently cerambycids, as well as inquiline residents of their mines, are major targets of aye-aye foraging behavior. The larvae bore extended mines that course approximately parallel to the long axes of the trees in which they reside. The orientation and large size of the mines offer an acoustical trail that the aye-aye may follow to its prey. © 1995 Wiley-Liss, Inc.     

Breeding aye-ayes: an aid to preserving biodiversity

In August 1992 an aye-aye Daubentonia madagascariensis (Primates) was bred in captivity for the first time. This species is the only living representative of a monotypic family and is endangered in its native Madagascar. A brief history of the captive breeding effort and a summary of the conservation problems facing the fauna, flora, and people of Madagascar is given. The role that a captive breeding programme for aye-ayes can fulfil as an aid to preserving biodiversity is discussed.     

Competition for dead trees between humans and aye-ayes (<Emphasis Type="Italic">Daubentonia madagascariensis</Emphasis>) in central eastern Madagascar

The destruction and degradation of forest habitats are major threats to the sustainability of lemur populations in Madagascar. Madagascan landscapes often contain forest fragments that represent refuges for native fauna, while also being used for firewood and timber by local human populations. As undisturbed forest becomes increasingly scarce, understanding resource competition between humans and wildlife in disturbed habitats will be increasingly important. We tested the hypothesis that Malagasy and aye-ayes (Daubentonia madagascariensis) compete for the limited number of dead trees in rainforest fragments at Tsinjoarivo, Madagascar. We surveyed 2.16 ha within five fragments (range 5–228 ha) surrounding human settlements to quantify the density of dead trees and traces of both human and aye-aye activity. Neither aye-aye nor human traces were distributed according to the availability of particular trees species, and aye-ayes and Malagasy apparently preferred several different species. Although overlap was recorded in tree species used, human use tended to be positively correlated with a species’ desirability as firewood, while a negative relationship was seen for aye-ayes. Both consumers used trees of similar diameter at breast height, but those used by aye-ayes tended to be older, suggesting that human use might precede usefulness for aye-ayes. Finally, the density of dead trees and aye-aye traces were highest in smaller fragments, but human traces did not vary across fragment size. Although further study is needed to better quantify the aye-aye diet in this region, these data suggest that aye-ayes and local people compete for dead trees, and this competition could constitute a pressure on aye-aye populations.     

Characterization and evolution of major histocompatibility complex class II genes in the aye-aye, Daubentonia madagascariensis

Major histocompatibility complex genes (Mhc-DQB and Mhc-DRB) were sequenced in seven aye-ayes (Daubentonia madagascariecsis), which is an endemic and endangered species in Madagascar. An aye-aye from a north-eastern population showed genetic relatedness to individuals of a north-western population and had a somewhat different repertoire from another north-eastern individual. These observations suggest that the extent of genetic variation in Mhc genes is not excessively small in the aye-aye in spite of recent rapid destruction of their habitat by human activities. In light of Mhc gene evolution, trans-species and allelic polymorphisms can be estimated to have been retained for more than 50 Ma (million years) based on the time scale of lemur evolution.     

Was the Oligo‐Miocene Australian metatherian Yalkaparidon a ‘mammalian woodpecker’?

One of the most striking examples of convergent evolution within mammals is the suite of anatomical specializations shared by the primate Daubentonia of Madagascar and the marsupial Dactylopsila of Australia and New Guinea. Having last shared a common ancestor over 125 million years ago, these two genera have independently evolved extremely similar adaptations for feeding on xylophagous (wood-boring) insect larvae. These include enlarged incisors to gouge holes in wood, cranial modifications to strengthen the skull against the stresses generated by wood gouging and elongate manual digits that are used as probes to extract the larvae. Elsewhere in the world, the same ecological niche is filled by birds (woodpeckers or morphologically convergent forms) that use their beaks for wood gouging. An extinct group of eutherian mammals, the apatemyids, exhibit very similar craniodental and postcranial adaptations to Daubentonia and Dactylopsila and presumably also occupied the woodpecker niche. A qualitative analysis of characters of the skull and dentition of the enigmatic Oligo-Miocene Australian metatherian Yalkaparidon – specifically its combination of very large, open-rooted incisors, zalambdodont molars and features to strengthen the skull against rostral bending – supports the hypothesis that it is probably a fourth 'mammalian woodpecker'. Discovery of the (as yet unknown) manus of Yalkaparidon will test this hypothesis by revealing whether any of its digits are elongate.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 1–17.     

贵州布依族、仫佬族和毛南族9对遗传性状的基因频率

对贵州布依族、仫佬族和毛南族1239例的9对遗传性状的基因频率进行了调查, 并对民族间基因频率差异进行显著性检验。结果显示: 卷舌和小指弯曲的显性基因频率高于隐性基因频率, 而叠舌、前额发际、发旋、耵聍、拇指类型、中指毛、环食指长则相反; 卷舌、叠舌、前额发际、耵聍、拇指类型、环食指长的基因频率在民族间差异较大, 而发旋、中指毛、小指弯曲则相对较小。     

Comparing the use of live trees and deadwood for larval foraging by aye-ayes (<Emphasis Type="Italic">Daubentonia madagascariensis</Emphasis>) at Kianjavato and Torotorofotsy,Madagascar

Aye-aye (Daubentonia madagascariensis) feeding behavior has become synonymous with deadwood foraging. However, deadwood is not always the most frequently used substrate, as some aye-ayes use live trees more often to access invertebrates. We sought to compare the frequency of aye-aye invertebrate foraging in deadwood and live trees to better understand their feeding behaviors. We followed two male aye-ayes at Kianjavato, a heavily disturbed habitat in southeastern Madagascar, from October 2013 to October 2014, and one male and one female aye-aye at Torotorofotsy, a continuous forest in eastern Madagascar, from July 2014 to December 2015. We collected feeding data by recording the behavior of a focal aye-aye every 5 min for a total of 373 h at Kianjavato and 383 h at Torotorofotsy. Our results showed no difference in the amount of deadwood used between the individuals. However, there was a significant difference in the amount of live tree feeding between the female at Torotorofotsy and one of the males at Kianjavato. We conclude that feeding on invertebrates in live trees is more important to aye-ayes than previously realized and that aye-ayes are exceedingly flexible in their invertebrate feeding behaviors, adjusting to their habitat by using various substrates.     

Seasonal differences in hair growth rates of captive aye-aye,red ruffed,and black-and-white ruffed lemurs

Hair can be an important source of biological information, providing a record of such things as pollutant exposure, hormonal levels, and stable isotope ratios. Hair as a biological sample is easily accessible, easily stored, and resists degradation. Analysis of hair is particularly useful when studying rare and endangered species, such as lemurs, since it can be sampled noninvasively. However, to better interpret the results of stable isotope or other analyses, it is important to understand hair growth rates. We measured hair growth rates in captive aye-ayes (Daubentonia madagascariensis), red ruffed lemurs (Varecia rubra), and black-and-white ruffed lemurs (Varecia variegata), both in winter (December 23, 2013, to January 13, 2014) and summer (July 10–31, 2013) at the Duke Lemur Center. Hair growth per week in all three species of lemurs differed significantly between the boreal summer and boreal winter. The aye-aye, black-and-white ruffed lemur, red ruffed lemur had a mean weekly hair growth of 0.195, 0.209, and 0.232 cm, respectively, in the summer. While the aye-aye, black-and-white ruffed lemur, and red ruffed lemur had a mean weekly hair growth of 0.239, 0.464, and 0.479 cm, respectively, in winter. We found no effect of age on hair growth rates, neither in the boreal summer, nor in the boreal winter for black-and-white ruffed lemurs and red ruffed lemurs. A pregnant black-and-white ruffed female displayed negligible hair growth during the northern winter, suggesting that pregnancy may affect the partitioning of resources away from such things as hair growth.     

The morphology of the intrinsic tongue musculature in snakes (Reptilia,ophidia): Functional and phylogenetic implications

Tongue musculature in 24 genera of snakes was examined histologically. In all snakes, the tongue is composed of a few main groups of muscles. The M. hyoglossus is a paired bundle in the center of the tongue. The posterior regions of the tongue possess musculature that surrounds these bundles and is responsible for protrusion. Anterior tongue regions contain hyoglossal bundles, dorsal longitudinal muscle bundles and vertical and transverse bundles, which are perpendicular to the long axis of the tongue. The interaction of the longitudinal with the vertical and horizontal muscles is responsible for bending during tongue flicking. Despite general similarities, distinct patterns of intrinsic tongue musculature characterize each infraorder of snakes. The Henophidia are primitive; the Scolecophidia and Caenophidia are each distinguished by derived characters. These derived characters support hypotheses that these latter taxa are each monophyletic. Cylindrophis (Anilioidea) is in some characters intermediate between Booidea and Colubroidea. The condition in the Booidea resembles the lizard condition; however, no synapomorphies of tongue musculature confirm a relationship with any specific lizard family. Although the pattern of colubroids appears to be the most biomechanically specialized, as yet no behavioral or performance feature has been identified to distinguish them from other snakes.     

蜂猴线粒体细胞色素b基因变异特点及系统发育分析

测定了蜂猴属（Nycticebus)1个蜂猴（N.coucang)和2个矮蜂猴（N,pygmaseus)个体的线粒体细胞色素b(cyt-b)基因全序列,比较现有的司猴科其他种序列,分析了核苷酸序列差异和碱基替换特点,以指猴为外群重建了系统发育树,结果表明,在所研究的个体中,2个蜂猴物种碱基组成具有哺乳动物的共同特点,它们之间转换比（特别是密码子第3位）是颠换比的6倍多,大于其他种间比较;低的Ka/Ks值（＜0．1）,说明懒猴科cyt-b基因的异义突位点受到强的选择压力作用。由cyt-b基因构建的系统发育树符合懒猴科化石记录和形态学分类观点,根据化石记录和与分化时间有一定线性关系的第3位颠换和同义突变速率,估算蜂猴与倭蜂猴种间,蜂猴与蜂属间可能的分化时间分别为300和600万年。