Sexual dimorphism in the walrus - male in the background, female in the foreground. Photo from www.marinebio.net.
Tusks in Odobenus rosmarus
Tusks in the modern walrus Odobenus rosmarus occur in
both sexes, but are generally larger and longer in males – and like most other
pinnipeds, they are polygynous (a single male mates with multiple females) and
sexually dimorphic (males are larger than females). The walrus is restricted to
the Arctic – and owing to this, tusks were usually
assumed to have something to do with ice. For example, walruses tend to use
their tusks to assist in hauling out onto ice, leading many to originally
propose that tusks evolved for this purpose. Other workers erroneously
identified tusks as being used for excavation of mollusks on the seafloor. However,
observations by Francis Fay (1982) and Edward Miller (1975) indicate that a use
in feeding or haul out behavior is unlikely. Miller (1975) studied aggressive
behavior in male walruses, and observed that tusks perform a central role in
male interactions. Most interactions consist of tusk threat displays – the
aggressor leans his head back so that the tusks are horizontal and pointing
toward the target. If the target is somewhat submissive the aggressor will
perform a “stabbing” motion. In more aggressive interactions the aggressor
strikes the target with the tusks using the same downward stabbing motion,
typically striking the hindquarters, back, or neck. These strikes commonly draw
blood but Miller (1975) doubted that many cause serious injury (similar to
elephant seal combat). Tusks were also frequently used to parry strikes close
to the face. Predictably, walruses preferentially threatened smaller males;
perhaps more adorably, juvenile males that even lacked tusks performed play
fighting that was similarly ritualized. Strikes tended to follow visual
threats, and Miller (1975) indicated that ritualized aggressive behavior like
this is fundamentally similar to that seen in sea lions, who perform visual
displays (prior to striking) by similarly leaning back and opening the mouth to
show the canines. Interestingly, the pattern of scarring is completely opposite
to the pattern of observed tusk strikes: scarring is mostly present on the
anterior neck region, and Miller (1975) attributed this to several reasons: 1)
his observations were on land and 2) during the summer. He hypothesized that
during the breeding season, more intense “face to face” combat on ice (or more
likely, in the water, as some rare anecdotes suggest) is the origin of anterior
scarring. So, the relatively violent behavior that Miller (1975) described is
not even that which is known to cause the most scarring on walruses – which
seems to suggest that walrus breeding behavior might be a bit terrifying and
may give the elephant seal a run for its money.
Walrus tusk display and combat. Threat displays frequently prelude tusk strikes. Photo from www.flickr.com
Many
earlier workers (see Fay, 1982: 134-135 and references therein) concluded that
walruses dug prey items out of seafloor with their tusks, and this was based
primarily on observations of tusk abrasion in dead animals. At least one early
study suggested that walruses scraped the seafloor with their tusks in a posterior
direction, but later revised to a side-to-side motion as no abrasion exists on
the posterior side of the tusks. Some early reports did cast doubt upon these
hypotheses, as occasional individuals were identified as lacking tusks but of
otherwise healthy appearance. Fay’s (1982) classic study re-examined the
abrasion patterns, and concluded that the primary direction of sediment-tusk
interaction was from proximal to distal (e.g. base of tusk to tip), which
indicates that tusks are passively dragged through the sediment during benthic
foraging. Fay (1982) also indicated that tusks are frequently used for
locomotion – including hauling out onto sea ice, and even during aquatic
sleeping with the tusks hooked over the edge of an ice floe (like a swimmer resting
at the edge of a pool). However, he suggested that these were secondary
functions and that by far and away the most significant functions were all
social in origin. He hypothesized that because all/most pinnipeds are
polygynous, the capability for tusk development is probably universal among the
group but extreme canine enlargement is probably only possible once a pinniped
lineage has made the shift from piscivory (fish eating) to suction feeding.
Notably, most toothed whales with tusks (beaked whales, narwhal, Odobenocetops)
are all either known or inferred to be suction feeders.
Abrasion of walrus tusks - figure from Fay (1982). Abrasion is focused on the anterior side of the tusk, indicating passive dragging of the tusks through sediment during foraging rather than active digging.
Temperate and Subtropical tusked walruses
Further eroding ice-related hypotheses for the evolution of
tusks in walruses are discoveries of fossil walruses that inhabited drastically
warmer waters than the extant Odobenus rosmarus. The earliest known
temperate tusked walrus was Alachtherium, which for the past 130 years
was known from Belgium,
and in the late 1990’s was also reported from the northwestern coast of Africa
(Geraads 1997). Subsequently, additional discoveries indicated more occurrences
of Alachtherium from Japan
and the eastern USA
as far south as Florida, and
records of the toothless odobenine walrus Valenictus from southern California
and even Mexico
(Deméré, 1994). Fossils of Valenictus from San
Diego and the Imperial
Desert indicated to Deméré (1994)
that walrus tusks evolved long before walruses became ice-bound in the Arctic,
and that tusks are thus “structures with history”.
Life restoration of Odobenocetops by Smithsonian artist Mary Parrish.
The walrus-faced whale Odobenocetops: implications
for tusk use
The 1990 discovery of a bizarre fossil mammal, named in 1993
by Christian de Muizon as Odobenocetops, led to a reinterpretation of
tusk function in walruses. Odobenocetops was collected from late-Miocene
strata of the Pisco Formation of Peru and initially accidentally misidentified
as a walrus; I’ve been told that an early SVP abstract with this mistake can be
found. LACM Curator Emeritus takes credit for setting the record straight and
asking those involved “why does the skull have premaxillary sac fossae?” These
fossae, for the uninitiated, are unique to odontocetes (toothed whales), and
Muizon (1993) named it as a new genus and species in a new family,
Odobenocetopsidae, which he and others (Muizon et al., 2002) considered to be a
sister clade to the Monodontidae – the family that includes the beluga and
narwhal (and the fossil belugas, Bohaskaia and Denebola). I won’t
go into too much detail irrelevant to the tusks, but Odobenocetops only
possesses two teeth: asymmetrical left and right tusks that are posteriorly
directed and set into elongate, columnar alveolar processes, and exhibits a
deeply concave palate. These features and their similarity with the modern
walrus indicated a similar mode of feeding. However, the occurrence of similar
tusks in a completely different type of marine mammal that independently
evolved benthic suction feeding for mollusks begs the question: did tusks
really evolve for social purposes? Muizon et al. (2002) conclude that the
orientation of the tusks is a bit too coincidental, and that the alveolar
processes likely behaved as “sled runners” to stabilize and properly orient the
head of Odobenocetops as it trawled the ocean floor for molluscan prey.
They conceded that the asymmetry of the tusks (the left tusk is barely erupted
while the right tusk is very long – up to 1.35 meters in Odobenocetops
leptodon; Muizon and Domning, 2002) indicates that such a function was not
optimized in Odobenocetops, and it likely reflects a social function
like the tusk of the narwhal.
Seafloor foraging of a walrus. From this paper by Levermann et al.
Speaking of tusked cetaceans… what the heck is the
narwhal tusk for?
This is a bit of a convenient topic to tack on here; I’d
like to revisit it in more detail in the future since some interesting papers
have come out in recent years on the topic. The narwhal (Monodon monoceros)
is also sexually dimorphic, and possesses a pair of tusks, generally only the
left tusk erupts from the soft tissue. Rarely males will possess an erupted
right tusk. Although formerly considered an incisor, recent CT studies indicate
that the tusk is embedded entirely within the maxilla and is therefore the
canine tooth; a series of other vestigial postcanine teeth also form (Nweeia et
al. 2012) but rarely erupt from the skull or soft tissues (and are therefore detectable
only using CT imaging). Sexual tusk dimorphism is a bit more extreme than in
the walrus: only 15% of female narwhals ever possess tusks that erupt from the
soft tissue, and the tusks are always smaller and shorter than those of males. Significantly,
narwhals do not appear to be polygynous. The narwhal tusk is conspicuously
“spiraled” (presumably for structural rigidity) and exhibits dentine tubules
exposed on the surface of the tooth – which suggests some ability to sense
water temperature and salinity (Nweeia et al. 2009). In contrast, in mammals
that masticate their food the dentine tubules do not extend to the outer margin
of the tooth; indeed, toothaches may be caused by dentine tubules being exposed
to the oral environment when a cavity forms. Additionally, a pulp cavity
extends along the entire length of the tusks. Field experiments which consisted
of exposing a small section of tusk to high salinity solution resulted in rapid
head movements and breathing in several different individuals. These
observations lead Nweeia et al. (2009) to propose that the narwhal tusk
fulfills a sensory function.
Male and female narwhals underwater. There are surprisingly few underwater photos of narwhals, although this is generally true of most arctic marine mammals and I for one don't blame photographers: it's damned cold! Photo by Paul Nicklen, National Geographic.
However, the above arguments follow for the narwhal: the
tusks are indeed dimorphic, and if these functions are not important for
females (85% of females lack erupted tusks, making sensory functions useless
for nearly half of the species), they probably do not reflect the main purpose
of the tusk. The extreme sexual dimorphism strongly indicates a social role,
and another recent study (Kelley et al. 2014) has found a strong correlation
between narwhal tusk size and testes mass – confirming the sexual/social
importance of tusks. More observations of tusk use in the narwhal is necessary,
but males have been observed rubbing or slapping tusks together, and broken
tips of tusks have been found embedded in other male narwhal heads (and, heads
of belugas) – indirect evidence of narwhal combat. Similarly, underwater
observations of walrus and narwhal behavior and combat are rare or lacking
altogether.
Adorable bonus photo (by Paul Nicklen, Nationa Geographic/Getty Images).
What about other walruses?
Thus far, almost all discussions of tusk evolution in
walruses have either been confined to the modern species, or daresay even
cetaceans like Odobenocetops. Obviously, the former is a necessary
starting point, and the latter merits consideration – but, what about extinct
walruses? The only serious consideration of tusk evolution using fossil
walruses was Deméré (1994), who (as outlined above) remarked upon tusks in
walruses (e.g. Valenictus) from temperate and subtropical latitudes. An important
question that hasn’t really been asked before is: who had the first tusks? The
answer is remarkably easy and quick: the dusignathine Gomphotaria pugnax,
which is 2-3 million years older than the earliest known tusked odobenine
fossils. Tusks in Gomphotaria are quite a bit different in morphology
than modern Odobenus: the tusks are short and procumbent, lack globular
dentine, and a smaller pair of lower tusks are present; similar double-tusks
are seen in Dusignathus (particularly D. seftoni). There is some
variation even amongst the odobenines: Protodobenus has thickened
maxillae and large canine roots, but the emergent canine crowns are barely
proportionally larger than that in a sea lion; tusks are absent in Aivukus, and
short, curved, and procumbent (forward inclined) tusks are present in Alachtherium/Ontocetus
and Valenictus (although somewhat longer but no less precumbent). Morgan
Churchill and I discussed a few of these points in our paper on Pelagiarctos
(Boessenecker and Churchill, 2013). This pattern tells us several things: 1)
“Sled runner” tusk function would have only really been present in the modern
walrus, as most earlier forms had somewhat procumbent tusks that would not have
been aligned with the seafloor; 2) tusks do not really seem to be correlated
with any subset of the marine environment, and association with ice likely
reflects a relatively recent (e.g. Pleistocene) adaptation of Odobenus
to high latitude environments; and 3) tusks evolved in several directions in
the last 8 million years, which if anything signifies sexual selection and
recalls horn and antler diversity amongst small clades of sexually dimorphic
and selective ungulates.
The moral of the story is this: there is a difference between what a structure evolved for and what its current function(s) is/are; when walrus tusks first evolved, there was no extensive pack ice and walruses inhabited temperate and subtropical latitudes. The walrus tusk continues to serve an important role in social behavior, but has been used for other purposes (locomotion, sleeping) and is thus an exaptation of sorts. This point can be extended to the narwhal: simply because the narwhal tusk can be sensitive to salinity and temperature does not mean that it evolved for that purpose. In both cases the evidence of sexual dental dimorphism is the most significant, and the evidence rather overhwhelmingly supports a social or sexual origin of tusks in both Arctic species.
References
R. W. Boessenecker and M. Churchill. 2013. A Reevaluation of
the Morphology, Paleoecology, and Phylogenetic Relationships of the Enigmatic
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Deméré, T.A. 1994. Two new species of fossil walruses
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