Our Bodies Were Not Built To Last

As summer kicks in to high gear, the weather is heating up, MLB pennant races are heating up, barbecue grills are heating up, and the music is reckless and hot. Last summer witnessed the 50^th anniversary of the Grateful Dead with an epic reunion and the 20^th anniversary of the passing of Jerry Garcia. Yet, unbelievably, the music never stopped and the long strange trip continues. The Dead have been resurrected once again, with Dead and Company rocking a six-week US tour. With my kids finally accepting their own fate as the next generation of Deadheads, the revival of the music that makes so many of us feel alive has gotten me thinking about heritability and what information (biological or existential) is critically important to pass on to the next generation. And further, what is the meaning of life? (Full disclosure: this could simply be how I am dealing with my own process of aging, so please humor me for a moment…)

 

Here’s a sobering thought: the fundamental meaning of life is to get your genetic material into the next generation. There is no deeper meaning from a biological perspective than to maximize reproductive fitness. Different species take different approaches to spreading their seed, so-to-speak. On one end of the spectrum, some animals like sockeye salmon and mosquitos, which live in relatively unstable environments where the probability of survival is relatively low, focus on producing large numbers of offspring before they die, hoping that these offspring will reach sexual maturity and also reproduce. This is a good reproductive strategy in such environments because reproductive fitness is defined not by one’s ability to pass on their own genes, but by their offspring’s ability to pass on their genes.

 

Contrast this with the approach at the other end of the spectrum. Some animals, like orcas and primates live in much more stable environments, in population densities that are near carrying capacity for the environment (the highest density that can be supported by the resources available). These species produce many fewer offspring, but because there is a high probability of survival for offspring and parents alike, the parents invest a considerable amount of energy into raising their offspring (I know this is true because my kids exhaust me! Please help…)

 

In the case of primates, in particular, we know a great deal about reproduction, life history, and parental investment: primates produce few offspring, invest considerable energy into offspring care, and they generally have lengthy lives relative to other species in the same habitats. Compound this with advances in modern medicine, and human primates are enjoying lifespans that increase with successive generations. We live longer than our grandparents’ generation, and so on and so forth. And while this is fantastic news because we get to enjoy our children and grandchildren for longer than at any other time during human history, this does not come without a significant price: our skeletons break down in ways that other primates’ do not. Simply put, our bodies were not built to last.

 

Humans are unique among primates in that we walk around on two legs. In fact, the evolution of our bipedal locomotion predated the evolution of our large brains by several million years. And our unique mode of locomotion combined with our ever-lengthening lifespans has resulted in several musculoskeletal problems that we develop as we age. Before we get to that somber topic, it is useful to review some of the anatomical adaptations that allow us to walk around bipedally.

1. Forward position of foramen magnum. The foramen magnum – or the opening in the skull through which the brain stem/spinal cord exit – is more anterior positioned in humans compared to other primates and mammals, which places the vertebral column directly underneath the skull as opposed to behind it as in quadrupedal animals.

2. S-shaped curvature of vertebral column. By moving the vertebral column directly underneath the skull, humans require an S-shaped spinal curvature (with cervical and lumbar lordoses and a thoracic kyphosis) in order to balance the head and torso over the pelvis.

3. Broad pelvis with laterally-flared iliac blades. The iliac blades of the human bony pelvis – the parts that stick out to the side – are rotated laterally and flare outward from the midline of the body. This positions the lesser gluteal musculature (gluteus medius and gluteus minimus) lateral to the hip joint, enabling these muscles to function as abductors of the thigh at the hip joint, and prevent excessive pelvic tilt to the unsupported side during the stance phase of bipedal gait. In nonhuman great apes, this musculature is positioned posteriorly and acts synergistically with the gluteus maximus to extend the thigh, not abduct it.



4. Oversized hip and knee joints. Joint loading in response to bipedal locomotion, as well as that reflective of body mass, is borne entirely through the joint surfaces of the lower limb in humans. Therefore, we evolved expanded articular surfaces compared to our great ape relatives, which reduces shear stress in the articular cartilage. The femoral condyles and tibial condyles of the human knee are also significantly flatter in lateral profile than in nonhuman apes, which further reduces shear stress in articular cartilage. Because articular cartilage is avascular and cannot actively repair itself, reducing the shear stress borne by the cartilage also reduces the incidence of damage.



Carrying angle of the femur

5. Carrying angle of femoral shaft. The shaft of the human femur (thigh bone) is oriented obliquely relative to the femoral condyles (the part of the femur that sits on the tibia, or leg bone, to form the knee joint). This angled shaft places the knee joint directly under the center of mass. In quadrupedal animals (including our great ape relatives), the femoral shaft is more vertically oriented.

6. Adducted hallux. The human hallux – or big toe – is in line with all other digits of the foot, enabling an efficient toe off in an anterior direction in bipedal gait. In nonhuman primates, the hallux is abducted, which enables these animals to grasp with their feet in a fashion similar to manual grasping.

7. Sesamoids in tendons of flexor hallucis brevis. Sesamoid bones are bones that develop in the tendons of muscles, and the best example is the patella, or knee cap. In humans, sesamoids also develop in the tendon of flexor hallucis brevis, a muscle in the sole of the foot that flexes the big toe. These sesamoids create a tunnel through which courses the tendon of flexor hallucis longus (another big toe flexor muscle). This tunnel allows flexor hallucis longus to remain free to contract and flex big toe when all of the body weight is placed on head of the 1st metatarsal, such as when pushing off during walking.

These seven adaptations to bipedal locomotion are present in the earliest members of the fossil genus Australopithecus (and some earlier ones too), even before brains evolved to be bigger. So one can make the argument that bipedal locomotion is the hallmark of human evolution, with the evolution of big brains being a secondary adaptation that may or may not be related to the evolution of our unique locmotor mode.

Numerous hypotheses exist as to why we evolved this weird form of walking. Walking around bipedally is energetically efficient; it requires only approximately 1 calorie/min to walk. Was this the advantage it proffered over quadrupedal locomotion? Or perhaps we became bipedal in order to free our hands up to carry provisions back to our mates. Or maybe it was a way of reducing heat stress by reducing the surface area where sunrays hit directly while increasing the amount of surface area exposed to wind? Could it have evolved in order for us to see over tall grasses in the savannah? Or to increase feeding efficiency and resource exploitation? Or perhaps it was so we could posture for mates… All of these are plausible hypotheses, and there are plenty of scientific arguments in favor or one or more of these. But the fact remains, it doesn’t really matter why we evolved bipedal locomotion. Any way you slice it, we evolved it. And now we’re saddled with the baggage of our ancestors: bodies adapted to bipedal locomotion take a severe beating. Again, our bodies, especially our skeletons, were not built to last.



Vertebral compression fracture

Bone is approximately 60% mineral (calcium and phosphate) and the other 40% is collagen and other proteins. We reach our peak bone mass at about 30 years of age, which means that the most responsive time for us to build bone mass is while we are young and growing. With age, everyone loses bone mass and density; we call this osteopenia, and it is normal. But when we lose an abnormal amount of bone mass, we can this osteoporosis. Osteoporosis is common, with about 54 million Americans suffering from this disease, and often results in bone fracture. The most prevalent osteoporotic fractures are vertebral compression fractures, where the loss of bone in the vertebral column results in fracture of the body of the vertebra itself. Humans and the other great apes have an equivalent amount of bone mineral and equal bone densities, but human vertebral bodies are enlarged to absorb more compressive shock during bipedal locomotion. Therefore, they have thinner walls of the vertebral body, which are at risk of collapsing with reduced bone mass and/or density, resulting in compression fracture. These types of fractures do not occur in nonhuman apes because they have thicker walls of their vertebrae than do humans, and because their spines are parallel to the ground, not perpendicular, so there is no axial compression of the vertebral column during locomotion.

Another result of repetitive compression loading of the spine that only humans suffer is degenerative disc disease. Intervertebral discs between each of the vertebrae of the spine are comprised of two tissue types: a central, jelly-like nucleus surrounded by a strong, fibrous ring that contains the nucleus. After repeated compression, the fibrous ring of the intervertebral disc can break down, leading to a posterior bulge that impinges upon peripheral nerves that exit the spinal cord (which runs through the canal in the posterior aspect of the vertebral column). Ergo, pinched nerves. These degenerated discs do not occur with high frequency in nonhuman apes, again as a result of their quadrupedal (and less destructive) mode of locomotion.

Degenerative disc disease

One final example of how our long lifespans are not in accord with the “lifespan” of our skeleton is degenerative joint disease and osteoarthritis. The ends of bones with joint spaces are covered in a thin layer of hyaline (articular) cartilage. Hyaline cartilage is avascular, meaning that it does not have its own blood supply, and it cannot actively repair itself if damaged. In order to protect against damage, joint surfaces (of the knee at least) become flatter as body size increases during growth. This is because as body mass increases, so does the transarticular load transmitted through joint surfaces (and hyaline cartilage covering them). This has the effect of reducing shear stresses that are experienced by the cartilage and limiting the capacity to damage the cartilage by growth alone. When the hyaline cartilage breaks down, the result is damage to the bone, pain, and joint swelling – osteoarthritis. The incidence of osteoarthritis in nonhuman great apes is dramatically lower than in humans, and is attributed to a combination of shorter lifespans in the wild and the lack of a destructive, bipedal mode of locomotion.

Given all of the ways that our skeletons break down during life, it is truly quite remarkable that 60-70 year old musicians such as the surviving members of the Grateful Dead are still able to shake it, shake it in the summer of 2016. So we should embrace it while we can keep on dancing, keeping in mind that while every cloud has a silver lining; in this case, every silver lining does have a touch of grey.

Contributed by: Jason Organ, PhD

Follow Jason on Twitter.

Jungers, W. (1988). Relative joint size and hominoid locomotor adaptations with implications for the evolution of hominid bipedalism Journal of Human Evolution, 17 (1-2), 247-265 DOI: 10.1016/0047-2484(88)90056-5


Jurmain R (2000). Degenerative joint disease in African great apes: an evolutionary perspective. Journal of human evolution, 39 (2), 185-203 PMID: 10968928


Latimer B (2005). The perils of being bipedal. Annals of biomedical engineering, 33 (1), 3-6 PMID: 15709701


Russo, G., & Kirk, E. (2013). Foramen magnum position in bipedal mammals Journal of Human Evolution, 65 (5), 656-670 DOI: 10.1016/j.jhevol.2013.07.007


Ward, C. (2002). Interpreting the posture and locomotion ofAustralopithecus afarensis: Where do we stand? American Journal of Physical Anthropology, 119 (S35), 185-215 DOI: 10.1002/ajpa.10185

Rushing To Help Limbaugh Understand Evolution

A terrible tragedy unfolded this week at the Cincinnati Zoo when a rare, 17-year old silverback gorilla named Harambe was killed by zoo officials who believed it was necessary in order to save a 4-year old boy who had fallen into the animal’s enclosure. News of this story spread far and wide and reaction from the public has ranged from outrage at the zoo to outrage at the parents of the child, and everywhere in between. Many primate and zoo experts have supported the split-second decision to take the life of the gorilla, interpreting the gorilla’s behavior as threatening to the boy. Cincinnati Zoo Director Thane Maynard said he stands by the decision: “We are heartbroken about losing Harambe, but a child’s life was in danger and a quick decision had to be made by our dangerous animal response team.” Yet, there are others who claim the decision was hasty and that non-lethal methods of dispatching the gorilla could have been employed. The debate will continue as more details about the situation come to light.

But an additional issue that arose during the coverage of this story can be clarified immediately, as the answer has been known for over 150 years. Yet surprisingly in 2016, some pundits still do not understand the basic fundamental concepts of evolution.

On his daily radio show on Tuesday, May 31, 2016, conservative talk show host Rush Limbaugh had this to say about the incident at the Cincinnati Zoo. In particular, Mr. Limbaugh chose to respond to the comments of Ashley Byrne, a spokesperson for the People for the Ethical Treatment of Animals, when she was interviewed on CNN’s Newsroom, saying:

ASHLEY BYRNE: “In many circumstances gorillas have shown that they can be protective of children or small beings.  Frankly, the fact that this gorilla was innocent in the first place, that's the first place that this situation went wrong because even under the best circumstances captivity is never adequate for gorillas and other primates. And in cases like this we see that it's even deadly. And this tragedy is exactly why PETA urges families to stay away from any facility, zoos, circuses, or otherwise, that displays animals as a sideshow for humans to gawk at.”

Mr. Limbaugh, after playing this audio clip responded this way:

RUSH LIMBAUGH: “This woman obviously has not read Genesis and even if she did, it wouldn't have any impact on her. But human beings travel all over the world to gawk at animals precisely because they're unusual! They're interesting. Some are cute, some are deadly, some...There's no way human beings are gonna not be interested in animals. Gawking at them out on safari, hunting them or what have you. By the way, you know there's another factor in this, Snerdley [call screener]? A lot of people think that all of us used to be apes. Don't doubt me on this. A lot of people think that all of us used to be gorillas, and they're looking for the missing link out there. The evolution crowd. They think we were originally apes. I've always had - if we were the original apes, then how come Harambe is still an ape, and how come he didn't become one of us? [switches to dopey voice] "Well, that's why we’re looking for the missing link, Mr. Limbaugh, your question is absurd."

By switching to a mocking tone, Mr. Limbaugh seeks to insult “the evolution crowd”, yet doesn’t seem to realize the joke is on him. Mr. Limbaugh’s comments reveal a striking ignorance about the most basic premise of evolution. Evolution does not state that we came from the gorillas, apes, or monkeys that you see today. Instead, we share a common ancestor with our fellow primate species – a common ancestor that lived long ago and has long since vanished.

Below is a phylogenetic tree representing the evolutionary relationships between the living primates. Humans (hominids) and chimpanzees are most closely related and, based on an abundance of molecular genetics and fossil data, it appears that humans and chimps diverged along their own evolutionary paths at least 6 million years ago (and possibly earlier).

This is a well-established fact that deserves repeating:  humans and chimps diverged along their own evolutionary paths. So while chimpanzees and humans share a common ancestor (technically, an ancestral population because an individual does not evolve; rather, populations evolve over vast periods of time), HUMANS DID NOT EVOLVE FROM CHIMPANZEES. Furthermore, gorillas diverged from the chimpanzee/human ancestral population even further back in time, approximately 7 or 8 million years ago. This is also why gorillas did not (and will not) become “one of us”.

This is why some in the “evolution crowd” might tell you that your question is absurd - it is a clear admission that you do not understand the key principle of evolution. Perhaps the analogy conveyed in this meme will clear up your confusion about how evolution works, and how humans actually evolved.

The discovery of evolution is one of the most revolutionary insights into who we are and why we are here. We implore Mr. Limbaugh and those of his ilk to reconsider whether they wish to continue believing in a fantasy, or have the courage to embrace reality. Many religious people do not see evolution as a violation of their faith; indeed, are you not insulting your creator by refusing to apply the reason that has been gifted to you?

Contributed by:  Jason Organ and Bill Sullivan

Follow Jason on Twitter.

Follow Bill on Twitter.

For more information about human evolution check out this series of podcasts from the Leakey Foundation.

References:

Venn, O., Turner, I., Mathieson, I., de Groot, N., Bontrop, R., & McVean, G. (2014). Strong male bias drives germline mutation in chimpanzees Science, 344 (6189), 1272-1275 DOI: 10.1126/science.344.6189.1272

Glazko, G. (2003). Estimation of Divergence Times for Major Lineages of Primate Species Molecular Biology and Evolution, 20 (3), 424-434 DOI: 10.1093/molbev/msg050

The Search For The Unicorn - Slightly Off-Center

Zootopia opened in movie theatres on March 4 and is on track to be another Disney classic. Among all the animals featured in this feature, you probably recall a few sporting horns...but did you happen to spot any unicorns?

The earliest writings that describe unicorns were those of the Greek, Ctesias, in the late 5^th century BCE. He described the Indian Ass, an animal with a white, strong body and perhaps a red head from which sprung a long single horn of red, white, and black. It was said that a cup made from the horn could neutralize any poison.

There are real animals with one horn, like the

unicorn leatherjacket fish in the top left, and the

Indian rhinoceros at the bottom left. The rhinoceros

beetle has one big horn and fairly large part of his

jaw below, so I don’t know if he counts. On the top

right is the Meller’s chameleon. They say he a has a

horn on his nose, but you have to look close and

want to see it.

Four hundred and fifty years later, Pliny the Elder, historian of Rome, also wrote about a very strong animal with a single horn protruding from its forehead. He described an oryx (an antelope with a single horn), an Indian Ox (probably a rhinoceros – rhino = nose and ceros = horn), and the same Indian Ass with a horse-like build and a single horn.

Pliny wrote, “The unicorn (uni = one, and ceros = horn) is the fiercest animal, and it is said that it is impossible to capture one alive. It has the body of a horse, the head of a stag, the feet of an elephant, the tail of a boar, and a single black horn three feet long in the middle of its forehead. Its cry is a deep bellow.” Uh-huh. That doesn’t sound much like an antelope or a rhino, so I guess he meant the Indian Ass.

Soon, Romans were trading long spiral tusks, but no one was telling where exactly they had come from. These “unicorn” horns were snow white with a tight spiral. As a result of these horns, the unicorn in the West settled down to be a pure white horse with a very long, pure white, spiraled horn. This is the image we generally see in tapestries and illustrations.

Kirin Beer from Japan uses a unicorn (kirin) as its

logo. Look closely and you can see the single

horn on its head.

In the Far East there were unicorns as well. Known as the qilin (pronounced chee-lin) in China, there was a version in Japan too, the kirin. This was a benevolent animal, with shiny scales like a dragon and one or perhaps two horns. It avoided fighting and walked so softly that it would not disturb or harm a blade of grass. An animal like this (perhaps the saola) is most likely the one referred to in the North Korea stories. In 2012, North Korea announced that its archaeologists discovered a unicorn lair. 

But back to the real world. Most likely, those horns in the Roman markets were really narwhal tusks, as discussed in a 2011 paper. It is very likely that the narwhal played into the unicorn legend, as their tusks could be offered as concrete proof of unicorn existence.

The narwhal (Monodon monoceros) is an amazing animal, and one that abandoned bilateral symmetry. Monodon means one tooth, and monoceros means one horn; a pretty accurate name, all in all.

Our post today uncovers many of the problems

with these cartoon narwhals. Yes, they love where

there is ice. But they don’t have all those teeth, the

tusk isn’t centered and doesn’t come out of their

forehead, and they don’t have a dorsal fin

to speak of.

Narwhals are a species of whale, meaning that they are mammals. They live way up north. From Baffin Bay, around Greenland, to the north of Russian, they swim in pods of 10-100, but you’ll rarely see them even if you live near there. There are perhaps 45,000-50,000 narwhals today.

This is a steady number because it’s so hard to get to where they live. Consequently, narwhals haven’t been hunted into extinction. They spend a lot of their time on deep dives under the ice floes, so they aren’t seen often. No narwhal has ever been seen feeding; we only know what they eat from examining stomach contents.

Their most distinctive feature is the long (up to 10 ft/3 m) tusk on the males. Just one tusk, mind you, like a unicorn horn. The narwhal tusk - like elephant, walrus or warthog tusks - is a tooth.

Very young narwhals have six maxillary (upper jaw) tooth buds and two pairs of tooth buds in the lower jaw (mandible). However, only one pair develops any further. A tooth bud is what you find on an X-ray of a child (see picture).

You can see the teeth developing from crown to

root in the darker tooth buds. The pulp is usually

dark, but the middle tooth has had a root canal

and a filling has been placed in the whole pulp

chamber. The large tooth to the left is the first

molar. It doesn’t have a baby tooth to push out

of its way.

Teeth form in the jawbones as tooth buds. Most narwhal teeth never go past the tooth bud stage, but occasionally a tooth will erupt where one shouldn’t. These are often misshapen or caught between the bone and the palate, or in the wrong place. This is all good evidence that the teeth are vestigial; they serve no functional purpose for the normal narwhal.

Just one tooth, almost always the left cuspid (most people call it a canine), does develop. Hold on though, it isn’t that simple. Instead of developing in a vertically directed tooth bud and erupting down through the jaw, the left canine stays horizontal and erupt right through the front of the jaw and through the narwhals lip!

Since the tusk is derived from the left cuspid, it erupts left of center, making the narwhal bilaterally asymmetric! A 2012 study showed that the bony attachment and length proves that the narwhal tusk is a canine, not an incisor as so many people think. But, it’s not just the location that makes the narwhal tusk amazing, it’s how it’s made and what it can do.

A 1988 study suggests that the tight spiral as it grows keep the tusk from curving. A curved tusk would make it hard of the narwhal to swim in a straight line. Whatever the reason, the spiral is an iconic image for both narwhals and unicorns.

The top image shows how the narwhal tusk is off

center. The bottom image is my analogy. The tusk

is offset like a knight with his jousting lance. This

is Heath Ledger in A Knight’s Tale. Um….why isn’t

he wearing armor?

Despite being a tooth, the tusk is quite flexible. It can bend up to a foot (0.3 m) in any direction without breaking. It’s awfully long, we said 10 ft. above, but most are in the 8-9 foot range. This is huge when you think that most male narwhals are only about 15 foot long in the body.

Teeth are normally built with the hard enamel on the outside. Enamel is harder than bone and protects the teeth from breakage when chewing. The mouth is a rough environment and teeth have to put up with a lot of abuse.

Deep to the enamel is a material called dentin. This stuff has a lot of similarity to bone, although it isn’t quite as hard and doesn’t have living cells within it (like osteocytes – see this post). The dentin does contain millions of tubules that go from the enamel junction all the way to the pulp in the center. The pulp has a nerve and blood vessels.

The dentinal tubules have fluid and small processes of the neuron in them. When you eat something cold or have a cavity, the fluid in these tubules moves and changes the pressure in the pulp chamber. The single neuron in the tooth is a pain neuron, so any pressure change is interpreted by your brain as pain. It teaches you to take care of your teeth, but it ain’t the most pleasant of all evolutionary adaptations.

The cartoon on the left shows the enamel crown

covering the dentin and the dentinal tubules.

Inside the tubules are the odontoblasts that lay

down dentin all during the life of the tooth and the

nerves that go into the tubules. The right image is

an electron photomicrograph of the tubules.

The narwhal tusk is different. It is the only tooth known that has the dentin on the outside, although a 1987 study showed that it has no enamel, so it isn’t really an inside out tooth. The dentin is covered by a thin layer of cementum. This is what normally covers the roots of the teeth and helps attach them to bone. The dentin of the narwhal tusk has about 10 million of those tubules, but it is different from human dentin.

A 1990 study compared calcium content and hardness between human teeth and narwhals. The narwhal cementum was more mineralized than human, but the dentin of narwhals was less mineralized than human dentin and was softer. This may be why the narwhal tusk is so flexible.

The tubules of the narwhal tusk dentin connect to channels in the cementum, so there is a communication to the outside. A group in 2014 showed this and used the information to hypothesize that the tusk is a mechanosensor. Experiments showed that their heart rate changed when the water touching the tusk was switched from freshwater to salt water. They hypothesize that the tusk senses temperature, salinity, pressure, and perhaps touch to help in navigation and hunting.

But if that’s the case, why do only males have them? Females have to hunt too. The group from the 2014 paper offers that males and females have sexually dimorphic foraging techniques – they eat different things and hunt differently, so females don’t need horns. This is not well-supported. Many scientists believe the long tusk is a sign of health and genes and is therefore an ornament for mate selection.

The dorsal fin of the narwhal is greatly reduced. It

has notches that scientists hope to use to identify

individuals. The lack of a dorsal fin is believed to

be so they don’t injure it on the underside of the

ice floes when they surface, but it could also be so

they don’t run it into the ocean floor as they feed

upside down.

Occasionally, one will see females with a tusk, but like with many tusked females (elephants, etc), they are usually shorter. You can also find narwhal males with two tusks. But two tusks doesn’t mean that they are returned to bilateral symmetry. Both tusks spiral to the left! There must be some strong left-hand genes at work.

One last thing. The offset tusk lead to another weird narwhal behavior. A group in 2007 put cameras and positional monitors on some narwhals and found that they tend to swim upside down a lot. Almost 70% of their time on the ocean floor was spent in the supine position. Since the tusk points down just slightly, scientists believe they hunt upside down so that the tusk won’t get stuck in the ocean floor and break! The tusk must be pretty important - or they just like lounging on their backs.

Contributed by:  Mark Lasbury, MS, MSEd, PhD
A version of this post was originally published on his blog, As Many Exceptions As Rules.

Christen AG, & Christen JA (2011). The unicorn and the narwhal: a tale of the tooth. Journal of the history of dentistry, 59 (3), 135-42 PMID: 22372187

Kingsley, M., & Ramsay, M. (1988). The Spiral in the Tusk of the Narwhal ARCTIC, 41 (3) DOI: 10.14430/arctic1723

Nweeia, M., Eichmiller, F., Hauschka, P., Donahue, G., Orr, J., Ferguson, S., Watt, C., Mead, J., Potter, C., Dietz, R., Giuseppetti, A., Black, S., Trachtenberg, A., & Kuo, W. (2014). Sensory ability in the narwhal tooth organ system The Anatomical Record, 297 (4), 599-617 DOI: 10.1002/ar.22886

Dietz, R., Shapiro, A., Bakhtiari, M., Orr, J., Tyack, P., Richard, P., Eskesen, I., & Marshall, G. (2007). Upside-down swimming behaviour of free-ranging narwhals BMC Ecology, 7 (1) DOI: 10.1186/1472-6785-7-14

For more information or classroom activities, see:

Narwhals –

http://oceanexplorer.noaa.gov/explorations/06arctic/background/edu/lessonplans.html

http://classroom.synonym.com/narwhal-endangered-species-6257.html

http://www.iucnredlist.org/details/13704/0

http://acsonline.org/fact-sheets/narwhal/

http://us-keepexploring.canada.travel/things-to-do/exp/arctic-kingdom-polar-expeditions-narwhal-polar-bear-safari#/?galleryItemId=200009872

http://betterlesson.com/lesson/604599/humans-vs-narwhals

http://www.lessoncorner.com/Geography/Countries/Greenland

http://southernmadeintheshade.blogspot.com/2012/01/nature-lesson-narwhals.html

http://video.nationalgeographic.com/video/weirdest-narwhals

http://www.discovery.com/tv-shows/human-planet/videos/capturing-a-narwhal/

http://www.bbc.co.uk/nature/life/Narwhal

http://www.pbs.org/wnet/nature/invasion-killer-whales-killer-whales-attack-pod-narwhals/11165/

http://www.smithsonianmag.com/ist/?next=/science-nature/in-search-of-the-mysterious-narwhal-124904726/

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

https://www.worldwildlife.org/stories/unicorn-of-the-sea-narwhal-facts

http://www.narwhal.org/

http://mentalfloss.com/article/55994/7-fascinating-facts-about-narwhals

https://whyevolutionistrue.wordpress.com/2012/04/22/mysteries-of-evolution-the-narwhals-tusk-or-rather-tooth/

https://whyevolutionistrue.wordpress.com/2012/04/22/mysteries-of-evolution-the-narwhals-tusk-or-rather-tooth/narwhal-teeth-vestigial/

Tooth structure –

https://thesebonesofmine.wordpress.com/2011/03/05/the-biological-basis-of-teeth-and-the-anatomical-directional-terms/

http://www.uic.edu/classes/orla/orla312/BHDI.html

https://www.youtube.com/watch?v=FiCPRvd6kT8

http://www.animated-teeth.com/questions-answers/dental-health-quizzes.htm

http://community.lessonplanet.com/t/what-big-teeth-you-have/1583

http://www.lion.co.jp/en/oral/role/01.htm

http://www.everydayhealth.com/dental-health/101/your-mouth-101.aspx