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Lemurs: the Ghostly Primate?

By Josie R Mills, on 9 June 2017

Did you know lemurs are primates? In fact they are one of the oldest primates, known as prosimians, which evolved long before monkeys and apes. They belong to the suborder Strepsirrhini alongside other mostly insectivorous and nocturnal primates like bushbabies, lorises and pottos. Lemur-like primates appeared in Africa around 60 million years ago and crossed the sea to Madagascar shortly after – possibly via rafting on clumps of vegetation or trees. Madagascar, which had separated from the super continent Gondwanaland 100 million years earlier, continued to drift further from the African Coastline; this meant that no other primates were able to cross to its shores. Consequently Lemuriformes continued to evolve on Madagascar with no pressure from other primates and it is the only place where they survive today!

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Lemurs have a distinctive elongated nose seen here on a red ruffed lemur

Without this competition and predation lemurs evolved across the island’s distinct ecological niches, which range from dense forests, to lakes and open areas. There are over fifty different species of Malagasy lemur who all evolved from the same common ancestor, which makes variation in their behaviour particularly interesting. Lemurs have started to adopt behaviours previously associated solely with Haplorrhine primates (monkeys and apes!), including activity in the day, frugivory, and the formation of complex social groups. Lemur groups operate a matrilineal structure where power rests with adult females and their female children. This is due to the practice of female philopatry where females always remain in the group they were born in whereas males leave. This behaviour is relatively unusual within the primate world!

However Madagascar did not remain an untouched paradise for ever, with the arrival of arguably the most destructive and dangerous primate (guess who?) by boat around 2,000 years ago. As humans settled on the island they began to cause damage to lemur habitats and started to hunt them for food. This resulted in the extinction of several species of lemur including the giant lemurs Megaladapis and Archaeoindris. These megafaunal lemurs could reach the size of a gorilla but were slow moving and well adapted to their niche habitats making them easy prey. Some skeletal remains have been found with cut marks indicating butchery by humans.

Lemur’s unique evolution, far from the pressures of living alongside other competing primates, has allowed them to expand their evolutionary niches. One great example of this is new sightings of them being active both during the day and night. This newly observed behaviour has been called ‘cathemeral’, literally meaning around the clock, indicating the ability to distribute activity throughout the 24-hour period. This is very unusual in primates but has now been documented in four species of lemur on Madagascar; it is observed elsewhere in some populations of South American owl monkeys Aotus azarii (Fernandez-Duque et al. 2001; Tattersall 2008). Interestingly being most active during the day (Diurnality) is seen as a fundamental transition in primate evolution; the move into the light associated with larger group size and gregarious social behaviour (Donati et al. 2013).

However lemurs are traditionally nocturnal; the name ‘lemur’ derives from the Latin ‘lemures’ meaning ghost or spirit, perhaps linked to their spooky call and haunting stare seen reflecting from the dense Malagasy forests at night. The lemur’s gaze looks distinctive in the dark due to a biological feature unique to nocturnal animals, the tapetum lucidum, a reflective layer present behind the eye that maximises any available light. This provides a key advantage to nocturnal species, both predator and prey. Look closely and you can even see it on your family cat! The presence of this adaptation in many lemur species suggests that it was a characteristic shared by their common ancestor.

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I know these are cats, but you get the idea! (Photo credit: Awwwcats)

 

So if lemurs have this specialised nocturnal adaptation why are we seeing them active during the day? This unusual change in several different species of lemur presents quite a conundrum and several adaptive factors have been suggested that may have been influential (see Curtis and Rasmussen 2006 for more info):

  • Temperate control: Being able to spread their activity throughout the day and night allows lemurs to avoid extremes of temperature; on cooler days they can feed and forage in the day and vice-versa on hot days. In this way they would save energy otherwise used to regulate their body temperature.
  • Maximising digestion time: Extremely folivorous (leaf eating) lemurs may improve their digestion by being active at different times.
  • Predator avoidance: Lemurs may have adopted cathemerality to avoid their main predator the Fossa (you may remember these scary critters from the movie Madagascar); a highly specialised and dangerous nocturnal predator.

Contrasting non-adaptive hypothesis

  • An evolutionary disequilibrium: This theory proposes that cathemerality is only seen when a distinct ecological pressure is lifted putting a primate population into an evolutionary disequilibrium. Proposed by Van Schaik and Kappeler (1996) who suggest that lemurs can be active during the day due to removal of their diurnal predators by the recent mass megafaunal extinction events in Madagascar.

Overall the idea of an evolutionary disequilibrium is not well supported as there are distinct adaptive benefits to cathemerality; equally lemurs have a stable relationship with their main predator: the fossa. It appears that cathemerality is closely linked to predation and may provide other physiological benefits, but it is particularly interesting when re-evaluating the evolution of diurnal behaviour. In this way it emphasises the complex and diverse process that influence primate evolution and how there is not a pan-explanation for how certain behaviours appear. It also reminds us that when interpreting primate evolution new previously unseen things are happening all the time. Here’s where if I was going to bore you I’d link it back to Neanderthals but I won’t… Instead a picture of me hanging out with red ruffed lemur… and do check out the lemur specimens in the Grant Museum!

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Red ruffed lemur at Artis Zoo in Amsterdam

 

References:

Curtis, D., Rasmussen, M. A. (2006). The evolution of cathemerality in primates and other mammals: a comparative and chronoecological approach. Folia Primatologica 77: 178-193

Donati, G., Santini, L., Razafindramanana, J., Boitani L., Borgognini-Tarli, S. (2013). (Un-)expected nocturnal activity in ‘diurnal’ Lemur Catta supports cathermarlity as one of the key adaptations of the lemurid radiation. American Journal of Physical Anthropology 150: 99-106

Fernadez-Duque, E., Rotundo, M., Sloan, C. (2001). Density and population structure of owl monkeys (Aotus azarai) in the Argentinean Chaco. American Journal of Primatology 53: 99-108

Tattersall, I. (2008). Avoiding commitment: cathemerality among primates. Biological Rhythm Research 39: 213-228

Van Schaik, C. P., Kappeler, P. M. (1996). The social systems of gregarious lemurs: lack of evolutionary convergence with anthropoids due to evolutionary disequilibrium? Ethology 102: 915-941

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