The functional significance of the erupted narwhal tusk has been the subject of conjecture and theory since the writings of Albertus Magnus in 1495 (Magnus, 1495). It has been thought to serve as an acoustic probe (Best, 1981; Reeves and Mitchell, 1981), possibly associated with sound transmission (Ford and Fisher, 1978; Best, unpublished B.Sc. Thesis, University of British Columbia, 1972); a thermal regulator (Dow and Hollenberg, 1977); a swimming rudder (Kingsley and Ramsay, 1988); a breathing organ; a spear for hunting or finding food (Vibe, 1950; Harrison and King, 1965; Ellis, 1980; Bruemmer, 1993); an aggressive weapon in interspecific fighting (Brown, 1868; Beddard, 1900; Lowe, 1906; Geist et al., 1960) or self‐defense against predators (Buckland, 1882; Gray, 1889: Freuchen, 1935); and a tool used for breaking the ice (Scoresby, 1820; Tomlin, 1967), digging (Freuchen, 1935; Pederson, 1960; Newman, 1971), or resting on ice (Porsild, 1918). Many studies describe the tusk as a secondary sexual characteristic used in aggressive encounters or intraspecific display (Lowe, 1906; Norman and Fraser, 1949; Miller, 1955; Silverman, 1979) associated with tusk fracture and head scarring (Porsild, 1922; Silverman and Dunbar, 1980), and to establish social hierarchy amongst males (Scoresby, 1820; Hartwig, 1874; Mansfield et al., 1975; Silverman and Dunbar, 1980; Gerson and Hickie, 1985).

Examining the narwhal tooth organ system through a multidisciplinary approach that combines studies of anatomy, morphology, histology, neurophysiology, genetics, and diet gives a more comprehensive view of its functional significance and highlights sensory ability as an added functional attribute.

Anatomy Narwhal teeth have unusual anatomical features. Among them are (1) a sinistral spiral morphology (Worm, 1655; Scoresby, 1823); (2) an extreme degree of tooth asymmetry in males, with a single left tusk expression and embedded right tusk (Sonnini and Buffon, 1804; Home, 1813); (3) an extreme expression of sexual dimorphism, with the male having an erupted left canine tusk reaching 2.6 m and the female commonly with right and left embedded tusks, often less than 33 cm (Sonnini and Buffon, 1804; Home, 1813); (4) a unique form of tooth asymmetry in a double‐tusked expression, since the morphology of the spiral remains sinistral for both left and right antemeres, and the left tusk is often slightly longer than the right (Worm, 1655; Sonnini and Buffon, 1804; Home, 1813); (5) a horizontal direction of eruption in both erupted and unerupted tusk forms (Linné et al., 1792: Egede and Wood, 1818); and (6) perforation of the tooth through the upper lip (Hampe, 1737; Brisson, 1756; Crantz, 1767; Donndorff, 1792). Though narwhal teeth share many anatomical characteristics with other tusked animals including a lack of enamel (Ishiyama, 1987), the presence of cementum, dentin, pulpal tissue and their associated structures (Seltzer and Bender, 2002; Berkovitz et al., 2002), and the presence of the maxillary division of the fifth cranial nerve associated with tooth innervation (Nweeia et al., 2009), they have many distinguishing features. Among them are a cementum layer overlying over the erupted canine (Nweeia et al., 2012) tusk, a patent network of dentinal tubules through the full thickness of dentin (Nweeia et al., 2009; Boyde, 1980; Locke, 2008), and pulpal soft tissues, extending the full length of the tooth, diminishing only in diameter with age (Pederson, 1931; Dow and Hollenberg, 1977; Nweeia et al., 2009). Initial scanning electron micrographs of the erupted male narwhal tusk reveal patent dentinal tubules that extend the full thickness of the dentin and correspond to lumina on the tusk surface. The tubules radiating outward from the dentin‐pulpal wall are similar to those of humans and other mammals in diameter, though the spacing is three to five times wider. Limited scanning electron microscopy (SEM) has been completed for other odontocetes, but suggests dentinal tubules are well occluded within the erupted portion of the dentinal layer for most odontocetes (Boyde, 1980). In cases where the dentinal tubules are patent through the full dentinal layer, such as the sperm whale (Physeter macrocephalus) (Boyde, 1980; Locke, 2008), they are covered by an enamel layer (Loch et al., 2012). Dentinal tubules have been described for other marine mammals, including the rough‐toothed dolphin (Steno bredanensis) (Miyazaki, 1977), pantropical spotted dolphin (Stenella attenuata) (Myrick, 1980), grey seal (Halichoerus grypus) (Hewer, 1964), hooded seal (Cystophora cristata) (Mohr, 1966) harbor porpoise (Phoecoena phoecoena) (Perrin and Myrick, 1980), short‐beaked dolphin (Delphinus delphis) (Gurevich et al., 1980), bottlenose dolphin (Tursiops truncatus), and pilot whale (Globicephala melaena) (Boyde, 1980; Locke, 2008), and the walrus (Odobenus rosmarus), hippopotamus (Hippopotamus amphibious), and killer whale (Orcinus orca) (Locke, 2008). Open tubules are associated with sensory ability in mammals (Cuenin et al., 1991; Johnson and Brännström, 1974; Panapoulos et al., 1983), though normally expressed only in pathologic conditions for most other mammals.

Histology Studies of nerve‐associated tissue in the pulp of odontocete teeth are limited, though helpful in understanding function (Holland, 1994). Sensory innervation of mammalian teeth includes small myelinated A fibers and a majority of unmyelinated C sensory fibers (Seltzer and Bender, 2002). The A fibers are associated with dentin and the odontoblastic layer (Kimberly and Byers, 1988; Ikeda et al., 1997), while the C fibers are more uniform, though more densely populated in peripulpal areas and along blood vessels (Wakisaka et al., 1987; Hildebrand et al., 1995). Both A and C fibers contain the neuropeptide calcitonin gene‐related peptide, or CGRP (Silverman and Kruger, 1987; Fristad et al., 1994). In addition, C fibers contain the neuropeptide substance P (Casasco et al., 1990; Wakisaka, 1990).

Gene Expression The presence of sensory‐associated genes in the pulp is an indicator for sensory function in mammalian teeth. Though there is a lack of genomic information for the narwhal, techniques are available to measure the gene expression profiles using a universal array platform to de novo sequencing that are informative to identify sensory‐associated genes associated with the pulp (Velculescu et al., 1995; Unneberg, 2003; Roth et al., 2004). Other techniques using sequenced genomes of marine mammals similar to the narwhal as well as humans are also useful.

Diet Evolutionary patterns of mammalian tooth anatomy and morphology are driven by diet (Anapol and Lee, 1994; Jernvall et al. 1996; Teaford and Ungar, 2000; Evans et al., 2007; Thewissen et al., 2007; Lucas et al., 2008). Thus, comparing the foraging habits of male and female narwhals can potentially provide useful information about the erupted male tusk. Previous dietary studies comparing male and female narwhals from the Baffin Bay population have found no difference in stomach contents between the sexes (Finley and Gibb, 1982; Laidre and Heide‐Jørgensen, 2005); however, smaller sample size of female narwhals has limited these analyses, and stomach contents can be biased since they only provide information on the most recent meal from a specific foraging area. Stable isotope and fatty acid analyses provide long‐term integrated dietary information to investigate if dietary differences exist between male and female narwhals in the Baffin Bay population. Both techniques investigate chemical signals in animal tissues which have incorporated isotopic and fatty acid values from their prey over various time frames, depending on the tissue. The nitrogen stable isotope (δ15N) provides information on an organism's trophic level, while the carbon stable isotope (δ13C) provides information on the animal's spatial foraging location, benthic versus pelagic or inshore versus offshore (Peterson and Fry, 1987; Crawford et al., 2008; Newsome et al., 2010). Fatty acids are transferred relatively unmodified from prey tissues to predator tissues, and thus can also be used to determine and compare diet among groups of organisms (Iverson et al., 2004). Both analyses have been successfully used to investigate diet in marine mammals (Iverson et al., 2004; Newsome et al., 2010) including walruses (Odobenus rosmarus) (Dehn et al., 2007), bowhead (Balaena mysticetus), and gray (Eschrichtius robustus) whales, and the narwhal's closest relative, the beluga whale (Delphinapterus leucas) (Horstmann‐Dehn et al., 2012). When the two analyses are used together and provide complementary results they can verify and confirm dietary interpretations, as was done in determining the primary prey for the beluga whale as arctic cod (Loseto et al., 2008, 2009) and for the bottlenose whale as Gonatus (Hooker et al., 2001).

Neurophysiology Brännström's theory of dental sensitivity is the most widely accepted mammalian model to explain this sensory ability and function for teeth. Changes to the interstitial fluid flow within dentinal tubules changes the conformation of odontoblastic cells connected to a pulpal nerve plexus which sends signals of sensory perception to the brain (Brännström, 1966). This theory explains the known ability of teeth to sense environmental stimuli, and supports the evolutionary descriptions of tooth precursors as sensory organs (Lumsden, 1987). Human and other mammalian teeth are known to be capable of sensing external stimuli (Anderson, 1968; Haegerstam, 1976; Byers and Dong, 1983; Byers, 1984; Balam et al., 2005) such as temperature (Yamada et al., 1968; Jyväsjärvi and Kniffki, 1987; Ahn et al., 2012), pressure (Mengel et al., 1992), proprioception (Hassanali, 1997; Catania and Remple, 2002; Ozer et al., 2002), osmotic gradients, galvanic potential (Ramirez and Vanegas, 1989; Heyeraas et al., 1994), nocioception (Hu et al., 1978; Lisney, 1983; Narhi et al., 1984; Shigenaga et al., 1986; Byers et al., 1988; Iwata et al., 1998; Kawarada et al., 1999; Andrew and Matthews, 2000), and percussion (Ogawa et al., 2002; Watanabe et al., 2003). Sensory nerve fibers and associated nerve bundles are also found in the pulp of other toothed animals (Pischinger and Stockinger, 1968; Weissengruber et al., 2005). This sensory ability serves many different functions, such as protecting teeth against environmental insults and responding to age‐related and pathological conditions (Hildebrand et al., 1995). Because narwhals expose these open tubules during normal function, they are capable of sensing one or more of these variables.