Biology

When The Early Bird Is Also The Night Owl

Biology concepts ? cathemerality, circadian rhythm, adaptation, predator/prey relations

One carnivorous and three vegetarian friends

stranded on a island ? what could go wrong?

The 2005 movie ?Madagascar? had some animals that we recognize from zoos; a lion, a zebra, a hippopotamus, a giraffe. But who were the bad guys? They were called the ?Foosa? but what kind of animal was the foosa? And who were those little primates they were trying to eat?

Being an island, Madagascar has developed ecosystems all its own. There are plants and animals that live there and nowhere else on Earth. This can lead to some interesting and exceptional behaviors and activities.

Tenrecs are a weird group. Different species can

be a few grams to over a kilogram, may have between

30 and 45 teeth, are related to elephants, and a have

a common anal and urogenital opening like birds. With

all that going on, being blue and yellow doesn?t seem

that weird.

Madagascar has its share of diurnal activity (daytime) and even more activity under the cover of dark (nocturnal). The streaked tenrec (Hemicentetes semispinosus, one of about 30 species) is crepuscular (active at dusk and dawn), so that activity pattern is covered as well. This black and yellow-striped cross between a hedgehog and a shrew (just by the looks of it, not by parentage) feeds on worms and other invertebrates. A study from early 2011 described a unique behavior from the tenrec, one that may cause us to include the cricket in the tenrec?s ancestry.

The quills on the tenrec come in two sizes, the long ones are for protection, but the shorter ones can be rubbed together to make high pitched (ultrasonic in many cases) sounds that can be used for communication or navigation. In the low light conditions of sunrise and sunset, scientists are considering the idea that tenrecs use stridulation (making sound by rubbing body parts against each other) to echolocate in their surroundings, similar to bats. They can also keep tabs on one another, communicating constantly with other tenrecs, even with a mouthful of worm.

The short spines on tenrecs are controlled by individual

muscles, so that one spine can be rubbed against another

to make noise.

Crickets, beetles, and some vipers stridulate, but the tenrec is a stridulating exception in two regards. One, it is the only mammal known to do so; and two, it is the only animal of any kind known to communicate both vocally and by stridulation. Madagascar would be a cool place to visit ? weirdness like this is around every corner.

Even though the tenrec is a Madagascar native, I didn?t see him anywhere in the movie. Some animals are too weird even to be believable in a cartoon about talking animals.

The movie did feature a primate group from Madagascar, one that had a penchant for dance. Lemurs (from Roman mythology, lemurs = ghosts) are playful and energetic, and some are even said to dance, but I don?t think they crave house music like in the movie. The Sifaka verreauxi is called the dancing lemur, as it is the exception to four legged motility among the lemurs. S. verreauxi walks on two legs, but the outward turn of their hips make them sway back and forth, like they are dancing.

Lemurs of the genus Sifaka bounce around on two

legs to cover ground quickly. This looks like dancing, and

probably gave the movie makers the idea to turn the

lemurs into a group of party animals.

In the movie, I saw no less than seven different types of lemurs, but in truth there are about 100 lemur species and subspecies live on Madagascar and the nearby Comoro Islands (and nowhere else). Together, they are a microcosm of Madagascar activity patterns. Some lemurs species, like the large Sifaka verreauxi, are diurnal, while the smaller species, like the aye-aye, are generally nocturnal. Some are even crepuscular, active at both dusk and dawn (so they are not vespertinal or matutidnal). But the weirdest types of lemurs are those that don?t show any of these patterns; in fact, they show no pattern at all! If that isn?t an exception, I don?t know what is.

The lack of an activity pattern does have a name, cathemerality (from the Greek, cat = complete and hemera = day). Cathemeral animals are active for periods of the day and/or periods of the night. In some cases, the periods of activity are driven by competition, when competitors are resting or prey is active. In other cases, periods of activity might be influenced by the seasonal temperatures or even the phase of the moon.

Whatever the stimulus, cathemeral (sometimes called metaturnal) animals can sleep day or night and hunt day or night, with no period of adjustment needed. African lions are cathemeral, driven by hunger and the success rates of their hunts, or by a need to conserve water.

In Madagascar, the red-fronted lemur (Eulemur fulvus rufus) is cathemeral in activity, as is the blue-eyed black lemur (Eulemur macaco flavifrons). Among primates, only humans and this species of lemur have blue eyes. However, the males have black hair while the females are reddish, so there is no chance of little blonde-haired, blue-eyed lemurs.

It is called the blue-eyed black lemur, so why is it

reddish-brown? This species is sexual dichromatic;

picture above is of a female, only the males are black.

The blue-eyed black lemur sees in color and is generally adapted to diurnal living; this is witnessed by the increase of its nocturnal activity when there is a full moon and with the nocturnal light level in general. However, the blue-eyed lemur has at least some activity spread across the 24-hour day all year round. This is one of three cathemeral patterns of lemurs in Madagascar lemurs.

A second cathemeral pattern is seasonally driven. In summer, when the daylight hours are greatest, it is enough for some cathemeral animals to limit themselves to daylight activity, but expand their active hours a bit during winter, so they are active in both day and night. This is driven by a need to find sufficient food.

The third cathemeral pattern is one in which there is mostly diurnal activity in one season and mostly nocturnal activity in another season. This may be driven by changes in temperature or perhaps resource availability. In Madagascar, the tropical climate ensures that food is always available, and the lack of a winter means that the temperature ranges between 60?F and 80?F all year round.

Many scientists believe that cathemerality may be an transient evolutionary middle ground, that all the species that display cathemeral activity are merely moving from diurnal to nocturnal, or the opposite direction. This is also known as an evolutionary disequilibrium hypothesis, as opposed to the idea that cathemerality is a stable evolutionary strategy. A recent study using genetic markers across time (phylogenetics) indicate that there was a common ancestor lemur that was cathemeral as far back as 9-13 million years. This would indicate that cathemerality is VERY stable. These results therefore suggest that the three cathemeral patterns are related to stable patterns predation risk or food gathering.

However, the diets of the red-fronted lemurs and the blue-eyed black lemurs are very different considering that they are closely related species, called true lemurs (eulemurs, eu = true). Red-fronted lemurs eat only leaves, while blue-eyed black lemurs eat fruits. But they are both herbivores, and are both potential meals for a predator. This would be a good reason for being cathemeral; the lemurs can just choose to be active when the predator isn?t. Great idea, huh? Well, Madagascar?s biggest predator apparently read the lemurs? playbook.

The fossa is not a cat, it is not a mongoose, it is not a monkey.

It is a predator and it is found only in Madagascar. It has

retractable claws, the same as all cats except the cheetah.

The fossa (pronounced foosa - get the connection to the movie?) is really Madagascar?s only big predator. It looks like a cat as it walks, and has retractable claws like most cat species, but its tail is as long as its body, like a monkey or a lemur. The fossa?s snout is more mongoose-like, as is the length of its body compared to the length of its legs. The film version of Madagascar didn?t do justice to the physical nature of the fossa; the bad guys in the movie pass for large cats.

The fossa spends much of its time up in the trees (it is arboreal) and chases the lemurs from tree to tree. Its long tail and sleek body design help it to move and maintain its balance as it moves through the branches. Most interesting, and an exception to mammal body design, the fossa?s outside digits on its rear paws are its biggest, this helps it to grasp the surfaces of the trees.

The long tail of the fossa helps it chase down

lemurs in the trees by improving its balance.

It also helps that the fossa hunts lemurs in

groups, using cooperative strategies.

Up in the trees we have the lemurs; some diurnal, some nocturnal, some crepuscular, and some cathemeral. What a buffet for the fossa! No matter what time he (or she) wishes to dine, there could be lemur on the menu, so the fossa has adopted cathemerality as well.

The movie was accurate in showing the fossas and lemurs active in both day and night now, but did the lemurs become cathemeral to get away from fossas? Maybe. The lemurs evolved before the fossa; were they cathemeral because they didn?t have to worry about predation, and a few species have stayed that way? Could be. Did the fossa become cathemeral to take advantage of the lemur smorgasbord? Nobody knows ?yet. You can be sure that there are scientists who support each possibility.

Whichever way it happened, it points out a wrinkle that few people consider. Some animals can actually change their activity pattern. The shift is often in response to some ecological or physiologic pressure. Skunks are crepuscular - except for males in the mating season - they become diurnal.

Another example is the short-eared owl of the Galapagos Islands. The owls are crepuscular on islands that have a predatory buzzard species, but on islands without buzzards, the owls are diurnal. Finally, some anole species change their activity pattern from diurnal to nocturnal as the temperature rises. Even their color can change from green to brown as the temperature changes.

These shifts in activity patterns occur often enough that they can?t be called exceptions, but the majority of animals do hold a single pattern throughout the year. As such, nocturnal animals interact with other nocturnal animals and the same with diurnal animals. This isn?t a tough concept to grasp, even the movie got it right. Unfortunately, some folks in 1880?s Hawaii just didn?t seem to understand, and they are still dealing with the problems it caused.

Griffin, R., Matthews, L., & Nunn, C. (2012). Evolutionary disequilibrium and activity period in primates: A bayesian phylogenetic approach American Journal of Physical Anthropology, 147 (3), 409-416 DOI: 10.1002/ajpa.22008

For more information and classroom activities on cathemerality, lemurs, or fossa, see:

Cathemerality ?

http://www.ips2004.unito.it/Sym_Curtis.html

http://www.ncbi.nlm.nih.gov/pubmed/16415576

http://www.hindawi.com/journals/ijz/2011/362976/

http://www.deepdyve.com/lp/taylor-francis/avoiding-commitment-cathemerality-among-primates-kyInyZRVTH

Lemurs ?

http://www.ncbi.nlm.nih.gov/pubmed/16415576

http://www.nhbs.com/lemurs_of_madagascar_diurnal_and_cathemeral_lemurs_tefno_160645.html

http://www.lemurs.us/basics.html

http://nationalzoo.si.edu/Animals/Primates/Facts/FactSheets/Lemurs/default.cfm

http://www.globio.org/glossopedia/article.aspx?art_id=49

http://www.pbs.org/edens/madagascar/class1.htm

http://www.magpi.net/Community/Programs/Madagascar-Conserving-Biodiversity

http://www.lemurreserve.org/programs.html

http://www.animalcorner.co.uk/rainforests/lemur.html

http://www.actionbioscience.org/evolution/roberson.html

fossa ?

http://animals.nationalgeographic.com/animals/mammals/fossa/

http://www.sandiegozoo.org/animalbytes/t-fossa.html

http://www.edgeofexistence.org/mammals/species_info.php?id=43

http://www.environmentalgraffiti.com/animals/news-one-weirdest-predators-earth-fossa

http://www.zooborns.com/zooborns/fossa/

http://www.pbs.org/wgbh/nova/madagascar/classroom/l2_intro.html

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