Iron Shrew: Sorex cinereus & Blarina brevicauda

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Small, but fierce:  Sorex cinereus next to the eye of a needle. Image credit: Yale Peabody Museum / Curious Sengi.

The tiny shrew is a fearsome creature, a ravenous beast constantly seeking out prey to fuel its metabolic fire.  It seems appropriate that the teeth of this assiduous hunter are a striking blood red.

The red comes from a pigment deposited in the enamel.  Tooth color has been traditionally used to distinguish between two subfamily groups of shrews, the red-toothed Soricinae and the white-toothed Crocidurinae.  Soricine shrews are a prolific group of insectivores with over 260 species spread throughout the world.  If there is a patch of well-watered greenery near you, it is likely that a shrew is on the hunt tonight.

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A feisty little conspiracy of shrews, Blarina brevicauda, gathered in a museum drawer.  Image credit: Yale Peabody Museum / Curious Sengi.

Pigmented teeth of various colors have been reported in different species of cyprinid fish (carps, minnows), lungfish, salamanders, frog (a fossil from the Eocene, 36 – 40 million years old), snakes, lizards, extinct early mammals, rodents, and shrews.  While the red teeth of soricine shrews have been undoubtedly known for centuries, only in recent years have scientists been able to reveal the details though nano-scale structural and chemical analyses.

The red is a result of an ultrafine-grained iron oxide called magnetite (Fe3O4) concentrated in the first 40 microns of the tooth enamel.  Magnetite was deposited during tooth development by ameloblasts, cells that secrete the protein precursors to enamel.

Shrew Tooth Cross Section Micro

Cross-section of a tooth from B. brevicauda imaged under a microscope.  Pigmentation is localized in the outer aprismatic layer of enamel.  Teeth have a hard cover of enamel composed of a crystalline form of calcium in a mineral called hydroxyapatite; the red-colored magnetite is distributed around those crystals of hydroxyapatite.  Dentine is a softer mineralized substance containing a higher percentage of organic materials.  Image credit:  Dumont et al. 2014.

The obvious question is why soricine shrews should have red, iron-containing teeth.  The familiar properties of iron would suggest that the presence of this material would make teeth stronger.  Scientists have proposed a number of hypotheses for the functional adaptation of having iron pigment in teeth such as increasing the hardness of enamel; increasing resistance to acids; increasing resistance to abrasive wear; reducing catastrophic cracking of teeth; and generating different wear rates in regions of the tooth to maintain sharp cutting edges.

A functional study by Strait & Smith (2006) on the Short-Tailed Shrew (Blarina brevicauda) found higher densities of iron in teeth — and individual tooth cusps — that were subject to more mechanical stress and consequent wear and fracture.  They found a “functionally significant pattern” in the molars of these shrews, where pigmented enamel showed the highest concentration of iron on the crushing and grinding cusps (the hypoconid and entoconid of the talonid, if you are into that sort of thing).  In contrast, the shearing cusps of those same molars had relatively low concentrations of iron.  In addition, of the three molars, the anteriormost first molar (m1) was the largest in size and the most iron-rich.  Usually, molars tend to increase in size from front to back.  The unexpected inversion of this pattern might be due to opportunistic omnivory in shrews.  These tiny mammals often take down large prey items.  In order to scarf down and begin chewing prey that exceeds the narrow gape of their jaws, the primary chewing surface was displaced forwards.  To deal with the challenge of the initial breakdown of prey, the first molar is hypothesized to have increased in size and strength.

Shrew Teeth Cusps

Illustration of the left lower jaw of the Short-Tailed Shrew, B. brevicauda,with (a) showing the extent of pigmentation in lateral view of the large procumbent incisor, small canine, single premolar, and three molars and (b) showing the same tooth row in occlusal (chewing) view with cusps labeled.  Iron concentrations were highest in the hypoconid and entoconid, least in the metaconid and paraconid.  Image credit: Strait & Smith 2006.

In terms of the material performance, Dumont et al. (2014) performed nano-scale indentation tests showing that pigmented enamel is harder than unpigmented enamel by an average of 30%.  Despite this seemingly large difference in hardness, this is well within the range observed in other mammalian teeth, meaning that the presence of iron pigment does not bestow any special super-shrew powers of tooth hardness.  Ultimately, the question of how the inclusion of iron pigments in teeth translates into strength is still unresolved.  The lack of conclusive evidence comes from the inherent complexity of studying biological material properties.  Teeth are surprisingly sophisticated composite structures and it is not always easy to predict how they will behave under different stresses and strains.

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Skulls of three individuals of B. brevicauda.  Note the patterns of pigment deposition on the occlusal (chewing) surfaces of the molars as well as the variation in color.  There is some evidence that the extent of pigmentation, especially of the incisors, is an indicator of the age of the animal, with lesser pigmentation suggestive of more wear and greater age.  Image credit: Yale Peabody Museum / Curious Sengi.

The essence of shrew life is eating.  Regardless of our human struggle to understand how iron oxide pigments confer strength to teeth, shrews are definitely consuming large amounts of tough and highly abrasive items such as insects, snails, and earthworms full of grit.  They consume anywhere from 80 – 125% of their body weight of this stuff, so the critical importance of controlling tooth wear is real.  Shrews grow and then lose their first set of teeth in utero, thus entering the world with only one set of teeth to last a lifetime.  There are anecdotal reports of adult shrews with worn down dentition being found out in the open, just dropping dead the moment their engines ran out of fuel.

This frenetic need to eat might explain why there are red-toothed soricine shrews and white-toothed crocidurine shrews.  There is plenty of circumstantial evidence that red iron pigments give soricine shrews an edge in the metabolic race.  Soricine shrews have much higher energy demands than crocidurine shrews, which might be related to their respective northern and tropical climate distributions.  It has also been observed that soricine shrews are specialized to support a fast, efficient metabolism:  higher chewing rates, more efficient reduction of food into small particles readily broken down by digestive enzymes, and jaw configurations allowing for greater variety and flexibility of movement compared to crocidurine shrews.  It would not be surprising if wear-resistant red pigmented teeth were included in this suite of adaptations as well.

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Skull of B. brevicauda. Image credit: Yale Peabody Museum / Curious Sengi.

Outside of soricine shrews, the other major group of mammals to exhibit pigmented teeth are the rodents.  The yellow or orange front teeth of rats and beavers are the most prominent examples.  Unlike shrews which have pigment across all their teeth, rodents restrict pigmentation to their perpetually-growing incisors.  Analysis on beaver teeth found the pigment to be a poorly crystallized ferrihydrite, another iron oxide but distinct from the magnetite found in shrews.  Pigmented teeth have also been found in the fossil record, not only in shrew and rodent ancestors, but in two unrelated groups of enigmatic extinct mammals known as Multituberculates and Apternodontidae, indicating this morphology has evolved a number of times independently.

Multituberculate Teeth 2

Multituberculate Teeth 1

Teeth from the Late Cretaceous (~70 Ma) multituberculate Barbatodon transylvanicus flaunting some impressive enamel pigmentation.  The large, serrated blade-like fourth premolar (p4) is characteristic of this extinct group of early mammals.  This is the earliest known occurrence of red teeth in mammals.  The oldest red-toothed shrew is Domnina gradata from the Early Oligocene (29 – 34 Ma) of North America, suggesting that tooth pigmentation is a basal ancestral trait for soricines.  Image credit:  Thierry & Codrea 2015.

It is an easy epithet to call our early mammalian ancestors “shrew-like creatures,” as though shrews are so dismissively small, indistinct, and full of stupidly unrealized potential to the point of cliché.  But shrews have traveled the evolutionary road for a long time and proved themselves to be as fascinating and formidable as any other.  Did I mention that they are also venomous?

Shrews Chew Through Trap

Sorex araneus (A, B, and C) and Neomys fodiens (D) are two soricine shrews native to the Netherlands.  They have both inflicted significant chewing damage on aluminum live traps used in a population study.  The author states that these traps are designed to last up to 30 years, but with the increasing number of shrews being captured and turning their toothy fury upon their prisons, these traps can last no more than 5 to 10 years.  Image credit: van Boekel 2014.

 

References

Dumont, M., T. Tütken, A. Kostka, M.J. Duarte, & S. Borodin.  2014.  “Structural and functional characterization of enamel pigmentation in shrews.”  Journal of Structural Biology 186:  38 – 48.

Furió, Marc, J. Agustí, A. Mouskhelishvili, O. Sanisidro, & A. Santos-Cubedo.  2010.  The Paleobiology of the Extinct Venomous Shrew Beremendia (Soricidae, Insectivora, Mammalia) in Relation to the Geology and Paleoenvironment of Dmanisi (Early Pleistocene, Georgi).”  Journal of Vertebrate Paleontology 30 (3):  928 – 942.

Holman, Alan & D.L. Harrison.  2003.  “A new helmeted frog of the genus Thaumastosaurus from the Eocene of England.”  Acta Palaeontologica Polonica 48 (1):  157 – 160.

Jin, Chang-Zhu & Y. Kawamura.  1996.  “A new genus of shrew from the Pliocene of Yinan, Shandong Province, northern China.”  Trans. Proc. Palaeont. Soc. Japan 182:  478 – 483.

Miles, A.E.W.  1963.  “Pigmented Enamel.”  Proceedings of the Royal Society of Medicine 56 (10):  918 – 920.

Smith, Thierry & V. Codrea.  2015.  “Red Iron-Pigmented Tooth Enamel in a Multituberculate Mammal from the Late Cretaceous Transylvanian ‘Hateg Island.'”  PLoS ONE 10 (7):  e0132550.

Strait, Suzanne G. & S.C. Smith.  2006.  “Elemental analysis of soricine enamel:  pigmentation variation and distribution in molars of Blarina brevicauda.”  Journal of Mammalogy 87 (4):  700 – 705.

van Boekel, Wim H.M.  2014.  “Damage to Longworth live-traps by shrews.”  Lutra 57 (1):  39 – 42.

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