Endless Forms

Cutting edge news about discoveries in ecology, evolution and conservation.

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The Lemur Underground


From bears slumbering in their dens to frogs sinking into muddy tombs of suspended animation, a wide spectrum of animals use hibernation to survive inhospitable seasons.

We tend to associate hibernating creatures with cold, wintry environments – just a mention of hibernation conjures images of snow-blanketed forests and ice-covered ponds. A group of small tropical primates is breaking the trend, however—recent research has revealed that dwarf lemurs in Madagascar hibernate for up to eight months of the year.


Madagascar (in red box)


Cheirogaleus crossleyi

While scientists already knew that that the western fat-tailed dwarf lemur (Cheirogaleus medius) spends seven months of the year hibernating in tree holes (Dausmann et al. 2004), until recently there was no evidence that any other primate species on earth undertakes significant hibernation periods. A recent paper in Nature’s open access journal, Scientific Reports, presents new evidence of hibernation in two other primate species, the Sibree’s dwarf lemur (C. sibreei) and the Crossley’s dwarf lemur (C. crossleyi), both of which occur in east-central Madagascar’s high altitude forests (Blanco et al. 2013). While it may not seem as though primates would need to hibernate on a tropical island, Madagascar’s mountainous regions can indeed experience temperatures that dip below freezing—a significant thermoregulatory challenge for a squirrel-sized primate. Thus, a research group from Duke University Lemur Center decided to see if the overwintering strategies of eastern dwarf lemurs resembled that of the western species.

The researchers managed to trap dwarf lemurs prior to hibernation season, and outfitted each animal with a collar that featured both a radio transmitter and a temperature sensor. The collars allowed the animals to be located after they had retreated to their hibernacula, in addition to tracking fluctuations in body temperature while the lemurs were hibernating.


Eastern Madagascar

The researchers found that not only do these tropical lemurs hibernate for 3-6 months out of the year, the arboreal creatures actually spend their hibernation underground, despite their lack of adaptations for a fossorial (digging and burrowing) lifestyle. The lemurs nestled 10-40 cm (4-16 inches) beneath a the forest’s floor of secondary roots and humus, no small feat for an animal that appears to be optimized for life in the treetops. Each lemur denned up alone, and they used just one or two hibernacula sites per season.

This underground hibernation habit is intriguing; the other lemur species known to hibernate, C. medius, uses tree hollows exclusively. The researchers suggest that this difference in hibernation sites could be partially due to constraints imposed by soil type: soil in C. medius’ habitat is hard and dry, unlike the soft soils of the eastern forests. Another interesting point about hibernacula choice is that the eastern species use tree hollows, rather than burrows, for their normal resting periods during the non-hibernation season, meaning that hibernation is an event with a very specific site selection pattern, rather than just an extended rest in their usual shelters.

Temperature data from the collars showed that C. sibreei and C. crossleyi tend to keep their body temperatures more stable than C. medius, which may highlight another advantage of subterranean hibernation. Soil provides more resistance to ambient temperature fluctuations than hollow trees, meaning that the eastern species are better insulated during hibernation than their western relative.

A final noteworthy aspect of this study is that C. sibreei and C. crossleyi are basal species (less derived than many other species) within their branch of the lemur phylogeny. This raises the question of whether their hibernation patterns may be an ancestral condition for dwarf lemurs. In the mean time, you never know what could be underfoot in the forest . . .


Blanco, M. B., Dausmann, K. H., Ranaivoarisoa, J. F., Yoder, A. D. 2013. Underground hibernation in a primate. Science Reports. 3:1768.

Dausmann, K. H., Glos, J., Ganzhorn, J. U., Heldmaier, G. 2013. Hibernation in a tropical primate. Nature. 429:825-826.




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From Carrion to Carriers: Crows Transmit Infectious Prions

Most of us recall learning the basic rules of protein structure and folding in high school science classes (if not, see neat interactive animations here). Basically, form equals function, and a protein must be correctly folded in order to perform its duties. The critical nature of this process cannot be overstated, and the results of misfolded proteins in the brain—also known as prions—can be gruesome.


Rabies, “mad cow disease,” foot-and-mouth disease, kuru, chronic wasting disease—all of these ghastly illnesses are caused by prions, which are more technically known as transmissible spongiform encephalopathies (TSEs). Foaming at the mouth, loss of muscle control, hallucinations, hydrophobia . . . the symptoms of prion disorders can lead to truly tragic and painful deaths, all ultimately due to a few misshapen proteins.

Despite the Hollywood-worthy symptoms of prion disorders, the most disturbing part of a TSE is the ‘T’ part: “transmissible.” The specter of such a devastating brain disease being passed from one individual to another seems like something out of a cheap horror novel—and yet it happens every day.

We typically think about TSE infections as resulting from direct contact with an infected animal. However, what if you could become infected simply from exposure to feces left by an exposed yet unsymptomatic vector? A recent PLoS ONE paper describes a study on passive transmission of infectious prions by crows, highlighting a form of prion dissemination that is little-known, yet potentially very important from a disease ecology perspective. What happens when prions can hitch rides on non-symptomatic, aerial hosts?

Crows are notorious scavengers, and feed upon carcasses that may have died from any number of traumas or diseases. It is already known that TSE diseases can be spread by the consumption of flesh: kuru, a lethal form of encephalopathy found amongst the Fore people of Papua New Guinea, is transmitted through ritual cannibalism during funeral rites. Given that prion disorders such as chronic wasting disease and rabies are not uncommon amongst wildlife, there is a realistic possibility that scavengers will be exposed to TSE-infected flesh. The risks to scavengers are obvious, but the hazards extend beyond these animals. Will the prion strains remain infective after the infected food has been digested and excreted? This is a critical question that must be answered if we are to understand the role that scavengers play in transporting pathogens from place to place after feeding on carrion.


In the recent experiment reported by VerCauteren and colleagues, 20 American crows (Corvus brachyrhynchus) were fed mouse brain material infected with scrapie prions, to simulate feeding upon prion-infected carcasses. Next, the researchers obtained feces samples from the birds, and injected them into lab mice (the CF+ treatment group) to see if the disease remained infectious after passing through the birds’ digestive systems. Another set of mice (the MB+ treatment group) was injected directly with infected mouse brain material—the same substance that had been fed to the crows.

The results were striking. There were a handful of fatalities due to toxicity from uric acid in the bird feces, but all of the mice that survived for at least three days after the inoculations  exhibited neurological dysfunctions characteristic of prion disorders. They also all tested positive for prion infection during their postmortem examinations.

Mice that were injected directly with mouse brain material (the MB+ group) developed neurological symptoms 15 days earlier than those infected through crow fecal material (CF+ group), suggesting that indirect infection may provide a smaller dose, although still enough to be ultimately lethal. Between 83-100% of the crows were estimated to produce feces capable of infecting mammals with the prion disorder.

It is important to keep these results in perspective. This study was designed to provide conservative estimates of post-digestion prion infectivity. The type of scrapie that was used in this study, the RML Chandler strain, is more sensitive to enzymatic activity than many others. This means that more robust strains of prion disorders may be even more infective after ingestion and excretion by birds – an ominous scenario indeed.

The implications of these results are important and fascinating. The takeaway message of this study was that prions can remain lethally infectious after they have been digested and excreted by an avian scavenger. Crows produced infective feces within four hours of feeding, and in that amount of time a crow can travel a nontrivial distance from its initial feeding site.

This kind of transmission by volant scavengers could turn a TSE outbreak from a local, individually transmitted event into a much broader outbreak. Further research on how long prions remain infective in the feces under different environmental conditions will provide additional insights into how avian scavengers may affect the transmission dynamics of these diseases.




Prion Remains Infectious after Passage through Digestive System of American Crows (Corvus brachyrhynchos). Vercauteren, K. C., Pilon, J. L., Nash, P. B., Phillips, G. E. , and Fischer, J. W. PLoS ONE. http://dx.doi.org/10.1371/journal.pone.0045774