As the results are based on information from 6 narwhals outfitted with Crittercam and DTAGs, the findings and discussions are based on a relatively small sample size and should be interpreted cautiously.

Narwhal orientation in the water column

The Crittercam and DTAG recordings revealed that the tagged narwhals spent a substantial period of time oriented in a supine posture as they swam. This was documented both by the orientation data from the tagged whales and by video footage of other whales that were swimming ventral side up along the sandy and flat bottom. The extent to which all supine time periods recorded by the DTAG corresponded to intervals spent near or along the bottom could not be determined, but the short segment of overlapping video and DTAG data suggested that this behaviour occurred independently of proximity to the bottom.

It is not evident why narwhals display this behavioural tendency of swimming upside-down as they dive. The orientation may relate to the transmission beam pattern of their echolocation clicks. The beam pattern of narwhal clicks has not been measured but the beam of the most closely related species, the beluga whale (Delphinapterus leucas), was oriented about 5 degrees above the plane defined by the animal's teeth [18]. The orientation of the melon towards the bottom may direct the sonar beam downwards where the prey is likely to be most abundant. However, no convincing acoustic evidence supports this hypothesis since echolocation indicative of foraging occurred only rarely in the corresponding acoustic recordings during this upside-down orientation and feeding was not observed on the Crittercam footage [see [19]].

The absence of a pronounced dorsal fin and its replacement with a shallower dorsal ridge allows the animal to manoeuvre more easily ventral side up closer to the inlet bottom. It is believed that this lack of a dorsal fin has evolved as an adaptation to navigate beneath ice-covered waters [1]. This explanation has been proposed for the absence of a dorsal fin among two other cetacean species that are also associated with dense pack ice: the beluga and the bowhead (Balaena mysticetus) whales [20, 21]. However, other species including the sperm whale (Physeter macrocephalus) described as having a "low, thick, and rounded or obtuse" dorsal fin and the finless porpoise (Neophocaena phocaenoides) and northern and southern right whale dolphins (Lissodelphis borealis and L. peronii, respectively) that lack pronounced dorsal fins do not always live in ice-covered environments [22–24]. According to Fish [25], the cetacean dorsal fin is used to provide balance, stability and maneuverability. In addition, the lack of a dorsal fin favours a flexible body. Cetaceans with such flexible body designs (e.g., Delphinapterus, Inia) hence sacrifice speed for manoeuvrability [25]. Given this discrepancy, it is possible that the dorsal ridge of the narwhal and these other cetaceans may facilitate certain aspects of their underwater movement behaviour including roll.

The distinctive tusk that is characteristic of the majority of subadult and adult males and the occasional female may also relate to the upside-down behaviour observed here. If an animal close to the bottom were oriented dorsal side up and attempted to bend its head downwards to orient its melon towards the bottom, the tusk would be in danger of hitting the ground. The large proportion of broken tusks (34%) from a large West Greenland sample suggests that the tusk is brittle [26, 27], and that the narwhals should be cautious of breaking their tusks. The upside-down orientation would allow the tusk to be positioned near the bottom to scare and subsequently guide demersal prey towards its mouth like a shovel. The use of the tusk in association with feeding has been suggested previously [27, 28], proposing that the tusk was used to uncover and root out prey along the bottom. The tusk is often worn down at the tip, suggesting that it occasionally has a less severe contact with softer bottom substrate (e.g. mud, sand or gravel). Scarring on the head and broken tusks have been linked to violent fighting between sexually mature males [29, 30]. However, some scarring of the head could also be a consequence of swimming upside-down close to the seabed. Female narwhals and immature males also have some head scars, albeit not quite as many as mature males [30]. Wounds from such injuries can heal, which is not the case for a broken tusk. Finally, the tusk, although oriented along the longitudinal axis of the body, is angled slightly downward [31]. The downward angle is believed to have evolved to reduce the likelihood of the tusk being damaged when swimming under ice. However, near the bottom, it therefore may be better for the narwhal to swim upside-down.

If the narwhal swam flat against the bottom with its dorsal side up, it would have the advantage of having its mouth closer to benthic prey than if it were upside-down. However, the lower jaw of a narwhal is fragile because it is hollow and thin-boned probably because it is used for sound reception, as suggested by Norris [32] and Norris & Harvey [33] for other odontocetes. An open jaw hitting a hard bottom at a speed of 12 m/s could cause substantial damage. Hence, protection of the jaw could be another reason for the upside-down swimming.

On the Crittercam footage, we observed supine behaviour among both male and females, suggesting that the explanations relating to the use of the sonar and a protection of the fragile lower jaw may be most relevant for both sexes. The role of the tusk in feeding cannot be obligatory since female groups are often segregated from the males during a large part of the year but are still able to obtain food [34].

This supine swimming behaviour has important implications for the longevity and durability of tags deployed on both the tusk and dorsal surface of a narwhal. Premature failure of such equipment may be explained by transmitter collisions with the bottom, a danger also associated with swimming in ice-covered waters.

Upside-down swimming in other whale species

Some attention has been paid in the literature to upside-down swimming in other whale species. Akamatsu et al. [22] reported observations of finless porpoises swimming upside-down but did not quantify that behaviour or determine whether it was related to depth and proximity with the seabed. The Amazon river dolphin (Inia geoffrensis) has been reported to sleep underwater in an upside-down orientation [35]. Fristrup & Harbison [36] presented two hypotheses about the function of the rolling behaviour in the context of prey detection and capture by sperm whales. They postulated that sperm whales locate their prey visually, either silhouetted against down-welling daylight or by scanning for bioluminescence produced by the movements of their prey. However, results from DTAGs on sperm whales in the Mediterranean Sea and Gulf of Mexico do not support either hypothesis [37]. No consistent upside-down behaviour in the roll data is evident when creaking and sperm whales generally feed at depths without light from the surface. The acceleration bursts measured in the DTAG data also contradict the expectations of the second hypothesis [37]. Miller et al. [37] reported that sperm whales actively altered their body orientation throughout the bottom phase of their dives with significantly increased manoeuvring while producing creaking sounds. The creaking sounds are thought to be bursts of echolocation pulses used for the final stage in a foraging sequence. Grey whales and some river dolphins also feed by turning sideways near the bottom. Woodward & Winn [38] used a DTAG to demonstrate that a feeding grey whale spent more than half of its bottom time rolled at an angle >45°. The Indus river dolphin, (Platanista minor) is reported to swim on its side near the bottom of the muddy river, echolocating more or less continuously [39].

The turning direction relative to the turning of the tusk

No clear preference for turning direction was found for any of the tagged animals. There has been speculation surrounding the left-sided helical geometry of the narwhal tusk, how it has evolved and whether its conformation is influenced at all by the behaviour of the animal [40–42]. If narwhals turned consistently in a clockwise direction, this biased movement might support such asymmetric growth. However, neither the Crittercam nor the DTAG revealed such a preference in rolling direction (i.e., clockwise or counter-clockwise), casting serious doubt on such an explanation. In contrast, the study on grey whales by Woodward & Winn [38] using DTAGs documented that 97% of these rolls were clockwise. This matches a report from Kasuya & Rice [43] indicating that the right side of the grey whale rostrum had fewer barnacles and more scrapes than the left side. They also reported shorter baleen on the right side than on the left in 28 of the 31 animals measured, suggesting that most grey whales roll to the right when foraging.