Cannibalism in Gray Mouse Lemur: A Case of Hannibal Lemur

Gray mouse lemur (Microcebus murinus). Photo from Stanford University

See that cute guy up there? That's a gray mouse lemur (Microcebus murinus). Aren't they cute? Gray mouse lemur are arboreal mouse-like lemurs found on the island of Madagascar. They are nocturnal and are considered "cryptic species" because they come out at night. Gray mouse lemur are solitary when foraging but sleep in groups inside tree holes during the day. They are omnivorous, feeding mainly on vegetation, invertebrates and small vertebrates. Gray mouse lemurs can also hibernate during the cool months, a unique characteristic for primates. In recent years, wild gray mouse lemur are hunted and trapped for the pet trade. *Cue my PSA* Primates of any kind do not make good pets. While these gray mouse lemurs are cute, they are not meant to be pets.

The world of primatology is once again rocked to its core with the discovery of yet another primate species that cannibalize it's own kind. OK, well maybe it's not that serious but that's just a hook for you to continue reading my post.

Reports and observations of meat-eating in primate species have surfaced in recent years through published literature. Most of these primate species have never been observed predating on mammals (they usually eat invertebrates). While many know that chimpanzees occasionally eat meat, each chimpanzee subspecies have different hunting strategies and hunt specific prey species. Chimpanzees (Pan troglodytes schweinfurthii) from Gombe Stream National Park were observed hunting and eating red colobus monkeys (Colobus badius tephrosceles) by Dr. Goodall while western chimpanzees (Pan troglodytes verus) in Fongoli have been observed hunting and eating lesser bushbabies (Galago senegalensis) by Dr. Pruetz. Gomes and Boesch have reported that male western chimpanzees (P. t. verus) would also use meat to barter for long-term mating with females. Reports of meat-eating in Sumatran orangutans (Pongo abelii) had only surfaced as early as this year by Hardus et al. (2012). 


Of course, meat-eating is fundamentally different than cannibalism. Cannibalistic individuals eat the flesh of conspecifics. "Meat-eating" in literature generally refers to a meat consumption between heterospecific. In non-human primates, one of the explanations of cannibalism is thought to be a coping response with food scarcity. If food resources are scarce, both mother and offspring will die due to starvation. As a survival strategy, the mother would cannibalize her offspring (which will die soon anyway) as a way of returning the caloric investment back to the female. Juvenile and infant non-human primates are usually observed cannibalized by their mothers. I have covered maternal infanticide in Sumatran orangutans (Pongo abelii) and moustached tamarins (Saguinus mystax) in this blog, although many more primate species have been seen cannibalizing their own offspring.

This little gray mouse lemur is going to town with the carcass of an adult female conspecific. 

Photo by Anni Hämäläinen (2012)

A recently published paper by Hämäläinen (2012) described a male gray mouse lemur (Microcebus murinus) cannibalizing an adult female conspecific. The author does not know how the female died, but posit that the female could have been killed by predators. However, since carcass of the female was not consumed, it is uncharacteristic for a predator to abandon its prey. The author also suggests that the male seen cannibalizing the female could not have been the predator since female gray mouse lemurs are more dominant than males.

On attempting the second focal session for this individual at 21:52 hr, I encountered her at the approximate same location as an hour earlier, but at this time I could see the reflection of the collar and approached to 10 m distance. I found that she was dead and her body was being fed on by a conspecific male. 

The carcass was hanging head down from a branch at 1.5 m elevation from the ground. At the time of discovery, the body cavity had been torn open and the internal organs eaten. The skull had also been broken and the brain consumed. Additionally, the flesh had been torn from one hind and one fore limb. The corpse was known to be fresh since the individual had been seen active earlier and when the body was recovered, rigor mortis had not yet set in. When sighted, the cannibalistic male was ferociously biting into the protruding spinal cord (Fig. 1, supplementary material) and continued feeding on the body (the spine, ribcage, and soft tissue) for approximately 20 min after sighting. 

After his departure, I collected the body and brought it into the field camp, where a veterinarian conducted an autopsy the following morning. The autopsy provided no further clues to the cause of death or the animal’s health status since all the vital organs were missing.

The author claims that this is the first ever reported cannibalism in gray mouse lemur and the first incident of adult conspecific cannibalism in non-human primates in literature. The significance of this discovery is not just that a gray mouse lemur is seen cannibalizing its own kind but in some way reflects the flexibility of their diet. This observation could also further elucidate the foraging strategies of this species. Gray mouse lemurs could have been scavengers but because they are a cryptic species, this behavior was never observed by scientists. The author posit that cannibalism might be an immediate way of accessing nutritional and energetic benefits, therefore is adaptive in the individual level.

For more about this paper, please see A Case of Adult Cannibalism in the Gray Mouse Lemur, Microcebus murinus by Anni Hämäläinen (2012) published on American Journal of Primatology (AJP). You can also read about it on Science, ScienceShot: Cannibalism Seen in Gray Mouse Lemur.

Meat-Eating in Sumatran Orangutans

Caught in the act. Mother and infant Sumatran Orangutan sharing their kill, a slow loris.
Photo from NewScientist.

Well, well, well ... it seems like we have another great ape species who can't stay on a vegetarian diet. I mean, who in their right mind would want be an obligate herbivore right? Right? Actually ... contrary to popular belief, orangutans are not strictly frugivores (fruit eater). They also subsist on plant parts (leaves, buds, flowers, bark, sap, etc) and the occasional bird eggs and insects. Thus it came as to no surprise for me that some orangutans have acquired taste for meat. A varied diet is a good diet. A flexible diet in response to scarce food resources is an even better diet! Yes, I'm looking at you Giant Panda. Eat something else will ya? Edit: A rep from Giant Pandas did confirm that they do eat something else.

Sumatran Orangutans (Pongo abelii) are not the first great ape to have a taste for meat. Chimpanzees (Pan troglodytes schweinfurthii) from Gombe Stream National Park were observed hunting and eating red colobus monkeys (Colobus badius tephrosceles) by Dr. Jane Goodall while savannah chimpanzees (Pan troglodytes verus) in Fongoli have been observed hunting and eating lesser bushbabies (Galago senegalensis) by Dr. Jill Pruetz.



A new paper published in International Journal of Primatology, Behavioral, Ecological, and Evolutionary Aspects of Meat-Eating by Sumatran Orangutans (Pongo abelii), by Hardus et al. (2012) describes 3 rare cases of meat-eating by a mother and infant dyad Sumatran Orangutans. This pair was observed eating slow lorises (Nycticebus coucang), which the authors posit that meat-eating is a fallback strategy when food source (ripe fruits) are scarce. 
The authors also touched on very fundamental yet intriguing questions about meat-eating and hominid evolution in this paper. What are the minimum time on chewing is necessary for an adult female Australopithecus africanus to reach its daily energy requirement when subsisting partially on raw meat?  How did meat became a substantial component of hominid diet?

A. africanus needs 1202–1507 calories per day for their daily energy requirement. By using the chewing rate of P. abelii as a model, the authors estimate that A. africanus have to chew about 2 hours on raw meat to achieve 25% of their caloric needs while the remaining 75% were subsisted from easier to chew food sources such as leaves and insects.  Raw meat does not seem to be an efficient way to satisfy caloric needs but seemed to be a "fallback" resource when other food source are scarce. As to when meat became a substantial component of hominid diet, it is probably after the "discovery" of fire by Homo erectus. Cooked meat are easier to chew and provides more nutrient than from raw meat. The rate of mastication also decreases because most fibers within raw meat are broken down after it's cooked.

Early hominin ate "seafood", possible reason for the expansion of the brain

Recent archaeological find in Koobi Fora, Kenya suggests that our early ancestors might have dined on "seafood" to compensate for the energy and nutrition needed for the expansion of the brain. The excavated site dates 1.95 million years ago, which predates Homo erectus, reveals distinct faunal remains (some with evidence of butchery) and Oldowan artifacts. Detailed in latest PNAS edition, archaeologist David Braun and his team found an assemblage of bones from terrestrial and aquatic animals such as fishes, turtles and even crocodiles along with stone fragments (Oldowan tools) that are thought to be used to cut these animals with.

Photograph and scanning electron microscope image of a reptile bone scored by cuts. Image from PNAS.

“These aquatic foods are really important sources of the long-chain polyunsaturated fatty acids and docosahexaenoic acid that are so critical to human brain growth,” said co-author and paleoanthropologist Dr. Richmond. “Finding these foods in the diets of our early ancestors suggests they may have helped to lift constraints on brain size and fuel the evolution of a larger brain.”

    - PhysOrg.com

Braun posits that if these early hominins indeed ate these terrestrial and aquatic animals (fishes, turtles and crocodiles), then they would have ingested enough calories and fatty acids needed for the expansion of the brain without having to scavenge for animal remains. Braun thinks that these small-bodied hominins would have avoided the dangerous risk of confronting with larger scavengers.

Read more:
Crocs and fish key to human evolution on PhysOrg.

Did Dining on Seafood Help Early Humans Grow These Big Brains? on Discover.

Fossils Suggest Menu That Made Humans Possible on Wired.

Early hominin diet included diverse terrestrial and aquatic animals 1.95 Ma in East Turkana, Kenya (Braun et al., 2010) on PNAS.

Insectivory in Geladas

Thought I'd share this interesting observation about desert locust outbreaks in the Guassa Plateau, Ethiopia.  Fashing et al. (2010) observed that geladas (Theropithecus gelada), Ethiopian wolves (Canis simensis) and thick billed raven (Corvus crassirostris) feast on locusts in large quantities during an outbreak and immediately after in the Guassa Plateau. Although geladas are highly specialized herbivores, the observation suggest a surprisingly flexible diet shift during these outbreaks.

I tried to access the article but unfortunately it is paid-only. (Thank you Michelle, from Spider Monkey Tales, for a copy of the article). Judging from the abstract, it seems that this observation was done only during the locust outbreak of June 2009. It would be interesting to conduct a continuous study of this phenomenon to see if this diet shift really is a trend, like the authors suggested.

Reference:
Fashing, PJ. Nguyen, N. Fashing, NJ. 2010. Behavior of geladas and other endemic wildlife during a desert locust outbreak at Guassa, Ethiopia: ecological and conservation implications. Primates Retrieved April 19, 2010, from http://www.springerlink.com/content/w34871337p7070l1/ DOI:10.1007/s10329-010-0194-6

Why Did Our Early Ancestors Ate Nuts And Seeds?

A team of researchers, led by Professor Gerhard W. Weber from the Department of Anthropology at the University of Vienna in Austria, thinks that our early ancestors (specifically the australopithecines) probably started eating nuts and seeds because they were hungry and that was the only food available.

These adaptations are important in an environment where food is scarce. While being able to adapt to new food source is important, it probably would not be possible if they can't process these foods mechanically (chewing and processing). Adaptations such as large molars, robust teeth or thick enamel (morphological adaptation) are also important. Read more here: European scientists crack the mystery of why we eat nuts.

Also read, The feeding biomechanics and dietary ecology of Australopithecus africanus by Strait et al. (2010)

Natural Selection In Great Apes Favor Those With Teeth That Can Handle Fallback Foods

Great apes (orangutan, gorilla and chimpanzee) depend on their teeth to get them through tough times when food is scarce. Natural selection favor individuals with teeth that can process fallback foods, foods that are harder than the great apes normal diet of fruits. The evolution of the thickness of enamel in great apes reflects the mechanical demand of their diet.

"It makes sense if you think about it," says GWU's Paul Constantino. "When resources are scarce, that's when natural selection is highly active in weeding out the less fit, so animals without the necessary equipment to get through those tough times won't pass on their genes to the next generation."

Read the Science Daily article, Among Apes, Teeth Are Made for the Toughest Times and The Influence of Fallback Foods on Great Ape Tooth Enamel by Constantino et al. (2009).

Global Warming Threatens Folivory Primates

Black and white colobus monkey, one of the folivory species threaten by global warming.

A paper by Korstjens et al. (2009) suggests that even an annual temperature rise of 2°C would threaten folivory primates because these species would be forced to spend more time resting than foraging for food. This paper, Resting time as an ecological constraint on primate biogeography, was published online on Animal Behaviour. Here's the abstract:

Time constraints can limit an animal's potential to survive in a given habitat and the maximum size of its group. Many studies have, therefore, investigated the ecological correlates of time allocated to travelling, foraging and vigilance. However, animals spend more time inactive than active, and understanding the determinants of this resting time may provide new insights into the habitat-specific time-budgeting problems that animals face. We analysed the environmental constraints that determine the minimum amount of daytime an average primate has to spend resting, using data from a wide range of ecologically different species. However, total resting time consists of two components: enforced resting time (imposed on the animal by ecological constraints) and free resting time (the time available for allocation to ecologically functional activities). We show that the ecologically important enforced resting time is determined by diet and annual temperature as well as by temperature variation. Our tests of the biological significance of this relationship show that enforced resting time distinguishes between locations that are suitable or unsuitable for particular genera. We show that an annual temperature increase of 2–4 °C would greatly increase enforced resting time, leading to serious time-budgeting problems for many species. The effect of changes to enforced resting time on the biogeographical distribution of species is especially strong for folivorous primates. This study shows that resting time is an important component of animal behaviour that can help us understand extinction risk and geographical distribution of taxa.

Read more about this paper on PhysOrg.com, African leaf-eating monkeys are 'likely to be wiped out' by climate change.

Meat May Be The Reason Why Humans Live Longer Than Apes

 Meat, that's what for dinner.

Ever wonder why humans outlive apes? The answer might be because we eat a lot of meat. Genes evolved in humans to adjust to a meat-rich diet helps fight diseases associated with aging such as cancer, heart disease and dementia. Not to mention, the expansion of brain size in the genus Homo is also attributed to an increase in meat diet. Check out the MSNBC article "Meat may be the reason humans outlive apes" and the paper "Evolution of the human lifespan and diseases of aging: Roles of infection, inflammation, and nutrition" by Caleb Finch on PNAS.

Even Howler Monkeys Think Veganism Is Whack (Sorry PETA)

Alright fine. Maybe these black and gold howler monkeys are not Whitney Houston and they don't think veganism is whack but new observation had shown that these howler monkeys actually raid chicken coop (or bird nests) for eggs. Yes, for food not to paint Easter eggs.

Male (left) and female (right) black and gold howler monkey . Flickr photo from lemai13

Thought to be exclusively folivores, the black and gold howler monkeys (Alouatta caraya) feed mainly on leaves, fruits and other parts of the plants such as flowers and bark. However, the population of black and gold howler monkeys in the forest of Rio Grande do Sul, Brazil had been observed eating eggs. "Alouatta is the most studied New World primate genus in the wild and there is not a single observation of intentional ingestion of animal matter in the literature", said primatologist Dr. Julio Bicca-Marques.

In 2005 Ms Helissandra Prates, a student of Dr Bicca-Marques, observed two juvenile black and gold howler monkeys (Alouatta caraya) licking the interior of a dove's nest at Estancia Casa Branca, a 2 ha orchard forest in Alegrete. The nest contained a broken egg shell. She later found evidence of egg remains in howler monkey dung collected from the orchard floor.

Then in 2007, Ms Muhle, another of Dr Bicca-Marques's students, witnessed howler monkeys eating birds' eggs at a separate woodland site at Beco Xavier. Over an eight month period, she recorded 19 separate instances of egg predation by a group of five individuals. All these later cases involved chicken eggs, which the monkeys stole from a chicken coop. While all five monkeys were seen to enter and investigate the coop, most of the eggs were actually eaten by a single subadult male.

-  Walker M. 2009. Monkeys 'reject vegetarianism'. BBC.

The evolution of egg-eating is localized in this population, leading researchers to think that it is a response to environmental conditions. There is a high density of howler monkeys living in a habitat with low food sources. Bicca-Marques et al. think that eggs act as a surrogate supplementary source of protein because of the low food diversity. The shift from folivory to omnivory reflects the flexibility of the black and gold howler monkey's diet. Watch the video of a black and gold howler monkey raiding a chicken coop.

Dr Julio Bicca-Marques and her colleagues from the Primatology Research Group published their findings in the International Journal of Primatology. The paper, "Habitat Impoverishment and Egg Predation by Alouatta caraya" is available in .pdf form through SpringerLink for free.

A quick Google search reveals that local zoos feed their black and gold howler monkeys meat and eggs such as Connecticut's Beardsley Zoo. Interesting. Coincidence?

This finding reminds me of the dietary shift and exploitation of new food sources in chimpanzees. We know that Gombe chimpanzees (Pan troglodytes schweinfurthii) prey on red colobus monkeys (Colobus badius tephrosceles) (Stanford et al., 2005) while savanna chimpanzees (Pan troglodytes verus) from Fongoli hunt lesser bushbabies (Galago senegalensis) using spear-like tool (Pruetz and Bertolani, 2007). Will we see more published paper about dietary shift and exploitation of new food sources? I guess it would have to be a trend as these primates lose more and more of their food sources and habitat. Perhaps those with a flexible diet will better adapt to their changing environment and ecology.

Sorry PETA. It seems that omnivory is in and veganism is out.

References:

Bicca-Marques JC. Muhle CB. Prates HM. De Oliveira SG. Calegaro-Marques C. 2009.
Habitat Impoverishment and Egg Predation by Alouatta caraya. International Journal of Primatology 30 (5):743-748. [doi:10.1007/s10764-009-9373-y]

Pruetz JD. Bertolani P. 2007.Savanna Chimpanzees, Pan troglodytes verus, Hunt with Tool. Current Biology 17(5): 412-417. [doi:10.1016/j.cub.2006.12.042]

Stanford CB. Wallis J. Matama H. Goodall J. 2005. Patterns of predation by chimpanzees on red colobus monkeys in gombe national park, 1982-1991. American Journal of Physical Anthropology 94 (2): 213-228. [doi:10.1002/ajpa.1330940206]

Walker M. 2009. Monkeys 'reject vegetarianism'. BBC. Retrieved September 30, 2009, from http://news.bbc.co.uk/earth/hi/earth_news/newsid_8270000/8270801.stm

No Sex Can do The Muriquis Harm

Muriquis feeding and resting. Photo from Primate Info Net.

The muriquis, or woolly spider monkeys live in the rain forest of Brazil. They are considered peaceful individuals but an intra-community lethal attack had left researchers to reconsider how peaceful these monkeys are and why such attack occurred.

The image of peaceful individuals mainly stemmed from the northern population. Leaves are abundant in the northern population, so these muriquis chew on leaves all day and males would patiently queue to mate with females. When food is abundant, animals tend to stay in the same place.

However, in the southern population, fruits tend to be more abundant. Generally, females need more caloric intake compared to males, so females from the southern population disperse from the group to find clumps of fruits unlike the northern population where everyone stays together to eat.

It is in the southern population that a gang of six male muriquis were observed attacking another male from the same group, brutally biting his face, body and genitals. The male died about an hour later.

A change in dietary habit might be the clue to why such assault happened, said lead researcher Mauricio Talebi of the Federal University of São Paulo-Diadema, Brazil. Social bonding also explains why a gang of males attacked another male. Due to lack of readily available mates, males may become frustrated, creating tension and aggression between individuals. Because muriqui males bond for life with male siblings and relatives, this facilitates gang attacks, said Filippo Aureli of Liverpool John Moores University, UK. This assault can be seen as aggression among non-kin males.

For more, read 'Hippy' monkey is a killer when starved of sex on NewScientist and Intra-community coalitionary lethal attack of an adult male southern muriqui (Brachyteles arachnoides) on Wiley Interscience.