Re-assessing the applicability of the Jarman/Bell model and Kay's threshold to the insectivorous aye-aye (Daubentonia madagascariensis).

OBJECTIVES: Jarman/Bell principle and Kay's threshold suggest that large animals should not be able to sustain themselves on insects. However, animals with specialized morphological and/or behavioral adaptations violate these assumptions. Male aye-ayes were recently identified as having an insectivorous diet despite weighing 2.5 kg. We further explored this diet/body size disparity by studying behaviors of an adult female and juvenile male aye-aye. MATERIALS AND METHODS: We collected behavioral data on an adult female and juvenile male aye-aye in Torotorofotsy, Madagascar from January 2016 to December 2017. We used instantaneous sampling to determine the frequency of feeding events and continuous sampling during feeding behaviors to assess duration of feeding bouts. RESULTS: Invertebrates comprised over 88% of the diet for both animals. A Wilcoxon signed-rank test found no significant difference in the female's feeding frequencies between the hot/rainy seasons and the cold/dry seasons. DISCUSSION: Our results support earlier findings that invertebrates are the aye-aye's main resource and corroborate that aye-ayes violate assumptions of the Jarman/Bell model and Kay's threshold. We suggest that the Jarman/Bell principle and Kay's threshold be used as supporting evidence and not to repudiate findings that do not conform to these guidelines.

The inside tract: The appendicular, cecal, and colonic microbiome of captive aye-ayes.

OBJECTIVES: The aye-aye (Daubentonia madagascariensis) is famous for its feeding strategies that target structurally defended, but high-quality resources. Nonetheless, the influence of this digestible diet on gut microbial contributions to aye-aye metabolism and nutrition remains unexplored. When four captive aye-ayes were unexpectedly lost to persin toxicity, we opportunistically collected samples along the animals' gastrointestinal tracts. Here we describe the diversity and composition of appendicular, cecal, and colonic consortia relative to the aye-aye's unusual feeding ecology. MATERIALS AND METHODS: During necropsies, we collected digestive content from the appendix, cecum, and distal colon. We determined microbiome structure at these sites via amplicon sequencing of the 16S rRNA gene and an established bioinformatics pipeline. RESULTS: The aye-ayes' microbiomes exhibited low richness and diversity compared to the consortia of other lemurs housed at the same facility, and were dominated by a single genus, Prevotella. Appendicular microbiomes were differentiated from more homogenized cecal and colonic consortia by lower richness and diversity, greater evenness, and a distinct taxonomic composition. DISCUSSION: The simplicity of the aye-aye's gut microbiome could be attributed to captivity-induced dysbiosis, or it may reflect this species' extreme foraging investment in a digestible diet that requires little microbial metabolism. Site-specific appendicular consortia, but more similar cecal and colonic consortia, support the theory that the appendix functions as a safe-house for beneficial bacteria, and confirm fecal communities as fairly reliable proxies for consortia along the lower gut. We encourage others to make similar use of natural or accidental losses for probing the primate gut microbiome.

Neoplasia in Three Aye-Ayes (Daubentonia madagascariensis).

Tumours diagnosed in three aged captive aye-ayes (Daubentonia madagascariensis), held in two different institutions, are described. A cerebral glioblastoma was diagnosed based on histological and immunohistochemical findings in one of the animals following initial presentation with bilateral mydriasis, absent pupillary reflex, head tilt and ataxia. A second animal was humanely destroyed due to impaired locomotion associated with spondylosis and a post-mortem diagnosis of cholangiocarcinoma was made based on histology with further confirmation with immunohistochemical labelling for cytokeratin 7. A third aye-aye suffering from dental disease was diagnosed with an oral squamous cell carcinoma following an excisional biopsy from a non-healing wound in the lip. Due to progression of the neoplasia the animal was humanely destroyed and post-mortem examination revealed the presence on an additional unilateral phaeochromocytoma.

Alcohol discrimination and preferences in two species of nectar-feeding primate.

Recent reports suggest that dietary ethanol, or alcohol, is a supplemental source of calories for some primates. For example, slow lorises (Nycticebus coucang) consume fermented nectars with a mean alcohol concentration of 0.6% (range: 0.0-3.8%). A similar behaviour is hypothesized for aye-ayes (Daubentonia madagascariensis) based on a single point mutation (A294V) in the gene that encodes alcohol dehydrogenase class IV (ADH4), the first enzyme to catabolize alcohol during digestion. The mutation increases catalytic efficiency 40-fold and may confer a selective advantage to aye-ayes that consume the nectar of Ravenala madagascariensis. It is uncertain, however, whether alcohol exists in this nectar or whether alcohol is preferred or merely tolerated by nectarivorous primates. Here, we report the results of a multiple-choice food preference experiment with two aye-ayes and a slow loris. We conducted observer-blind trials with randomized, serial dilutions of ethanol (0-5%) in a standard array of nectar-simulating sucrose solutions. We found that both species can discriminate varying concentrations of alcohol; and further, that both species prefer the highest available concentrations. These results bolster the hypothesized adaptive function of the A294V mutation in ADH4, and a connection with fermented foods, both in aye-ayes and the last common ancestor of African apes and humans.

Deciduous dentition of the aye aye, Daubentonia madagascariensis.

Until the 1980s all interpretations of the deciduous dental formulae of the unusual and endangered prosimian primate Daubentonia madagascariensis were based on a publication more than 125 years old [Peters, 1866a]. Rather than being based on original material all later interpretations were exclusively derived from Peters' figures and descriptions. A relatively recent attempt by Luckett and Maier [1986] to establish the true milk dentition of the aye aye was based on histological evaluation of a late aye aye fetus from the collection of W.W. Hubrecht that was chemically preserved at least 80 years earlier. The death of a newborn aye aye at the Duke University Primate Center in 1992 finally made the following new evaluation of the D. madagascariensis deciduous tooth formula possible. Using X-rays and dissection, it here is demonstrated that aye ayes have one incisor, one canine, and two premolars in both the upper and in the lower milk dentition. Therefore the deciduous dental formula of Daubentonia madagascariensis should read: $${{\hbox{1i}\cdot\hbox{1c}\cdot\hbox{2p}} \over{\hbox{1i}\cdot\hbox{1c}\cdot\hbox{2p}}}.$$ © 1996 Wiley-Liss, Inc.

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.

Anatomy and adaptations of the chewing muscles in Daubentonia (Lemuriformes).

The extractive foraging behavior in aye-ayes (Daubentonia madagascariensis) is unique among primates and likely has led to selection for a specialized jaw adductor musculature. Although this musculature has previously been examined in a subadult, until now, no one has reported the fascicle length, weight, and physiological cross-sectional area (PCSA) for these muscles in an adult aye-aye specimen. For the present study, we dissected an adult wild-born aye-aye from the Tsimbazaza Botanical and Zoological Park, Antananarivo, Madagascar. The aye-aye follows the general strepsirrhine pattern in its overall jaw adductor muscle anatomy, but has very large muscles and PCSA relative to body size. Fascicle length is also relatively great, but not nearly as much as in the juvenile aye-aye previously dissected. Perhaps chewing muscle fascicles begin relatively long, but shorten through use and growth as connective tissue sheets expand and allow for pinnation and increased PCSA. Alternately, it may be that aye-ayes develop fascicular adaptation to wide gapes early in ontogeny, only to increase PCSA through later development into adulthood. The functional demands related to their distinctive manner of extractive foraging are likely responsible for the great PCSA in the jaw adductor muscles of the adult aye-aye. It may be that great jaw adductor PCSA in the adult, as compared to the juvenile, is a means of increasing foraging efficiency in the absence of parental assistance. Anat Rec, 297:308-316, 2014. © 2013 Wiley Periodicals, Inc.

Morphology of the nasal capsule of primates--with special reference to Daubentonia and Homo.

Primitive mammals are considered macrosmatic. They have very large and complicated nasal capsules, nasal cavities with extensive olfactory epithelia, and relatively large olfactory bulbs. The complicated structures of the nasal capsule follow a relatively conservative "bauplan," which is normally easy to see in earlier fetal stages; especially in altricial taxa it differentiates well into postnatal life. As anteriormost part of the chondrocranium, the nasal capsule is at first cartilaginous. Most of it ossifies endochondrally, but "appositional bone" ("Zuwachsknochen") is also common. Many fetal structures become resorbed. Together, all surviving bone structures form the ethmoid bone, but cartilages of the external nose and of the vomeronasal complex can persist throughout life. We describe in detail the anatomy of Daubentonia madagascariensis based on a fetal stage (41 mm HL) and an adult skull was analyzed by µCT. We found that the nasal capsule of this species is by far the most complicated one of all extant Primates. We also describe older fetuses of Homo sapiens (35 and 63 mm HL) as representative of a derived primate. The most significant feature of man--and probably of all anthropoids--is the complete loss of the recessus frontoturbinalis and its associated structures. It can be demonstrated that the evolutionary reductions within the primate nasal capsule mainly affect those structures associated with olfaction, whereas cartilages that are important for the biomechanics of the facial skull of the fetus persist.

Receiver bias and the acoustic ecology of aye-ayes (Daubentonia madagascariensis).

The aye-aye is a rare lemur from Madagascar that uses its highly specialized middle digit for percussive foraging. This acoustic behavior, also termed tap-scanning, produces dominant frequencies between 6 and 15 kHz. An enhanced auditory sensitivity to these frequencies raises the possibility that the acoustic and auditory specializations of aye-ayes have imposed constraints on the evolution of their vocal signals, especially their primary long-distance vocalization, the screech. Here we explore this concept, termed receiver bias, and suggest that the dominant frequency of the screech call (~2.7 kHz) represents an evolutionary compromise between the opposing adaptive advantages of long-distance sound propagation and enhanced detection by conspecific receivers.