Killer whales, one of the species investigated in the study. Photo credit: Wayne Vogl.

Killer whales, one of the species investigated in the study. Photo credit: Wayne Vogl.

Every diving animal that depends on air to breathe faces the challenge of crushing pressures compressing every tissue in their bodies, including the lungs, as they descend. Elastic tissues, such as arteries, which expand to accommodate pressure surges above the surface, become vulnerable to compression as soon as an air breather leaves the surface. ‘A few years ago, we discovered that the mechanical properties of fin whale arteries were different from those of typical terrestrial animals’, says Margo Lillie, who – with colleagues, Robert Shadwick and Wayne Vogl from the University of British Columbia (UBC) Canada, and others – discovered that the arteries are remarkably resistant to collapse, which may protect them during a dive. However, the trio also realised that the distinctive bobbing swimming style of whales and dolphins – where they beat their tails up and down – might also place arteries under increasing pressure if the animals compress their abdomen with each downward tail beat. Intrigued by the possibility that the abdomens of these diving mammals may be under more pressure than had been realised, the team wondered whether the divers’ diaphragms might be reinforced in some way to withstand the additional abdominal pressure generated during each downward tail beat.

Together, the team collected over 20 whale and dolphin diaphragms over a 5 year period. ‘We relied heavily on a network of people who collect the carcasses of animals that stranded on the shore and we also got diaphragms collected as part of a Canadian biological sampling programme and a commercial whaling operation in Iceland’, says Lillie. Although it was possible to ship most of the organs back to Vancouver, Lillie, Shadwick, Vogl and Stephen Raverty from the Animal Health Centre, Canada, had to travel to Iceland to investigate the colossal 1.5 m-wide fin whale diaphragms.

‘Compared to the diaphragms of terrestrial animals, the cetacean diaphragms looked so complex and they vary from one species to another, so it took me a while to start seeing patterns’, admits Lillie. However, it eventually became clear that the animals’ diaphragms were reinforced with a network of stiff collagen fibres. ‘There is a lot of variation in the amount of collagen on the surface of the diaphragm’, says Lillie; ‘There was hardly any on the beluga and minke diaphragms, while the Dall's porpoise diaphragm was covered with it’, she adds. Suspecting that the amount of reinforcement was related to the strength of the species’ tail beats – and therefore their swimming speed – Lillie was pleased when she realised that the diaphragms of the fastest swimming species – the Dall's and harbour porpoises – were covered in the highest proportion of collagen (almost 60%), while the slowest species – the belugas, and fin and minke whales – had the lowest proportion of collagen (∼10%).

‘We were surprised how closely the amount of collagen correlated with speed. It means that collagen deposited on the diaphragm could be necessary to withstand increased abdominal pressures associated with swimming’, says Lillie. And when they compared the whale and dolphin's diaphragm structures with those of other diving mammals (seals and sea lions), which probably do not compress their abdomens when beating their tails from side to side, there was no evidence of the extensive collagen reinforcement. Reflecting on the discovery, Lillie says, ‘The evolutionary decision to swim by moving the flukes up and down instead of side to side appears to have altered the design of the diaphragm’, and now she and Shadwick are keen to find out how the increase in abdominal pressure has affected the return flow of blood through veins to these animals’ hearts.

Lillie
,
M. A.
,
Vogl
,
A. W.
,
Raverty
,
S.
,
Haulena
,
M.
,
McLellan
,
W. A.
,
Stenson
,
G. B.
and
Shadwick
,
R. E.
(
2017
).
Controlling thoracic pressures in cetaceans during a breath-hold dive: importance of the diaphragm
.
J. Exp. Biol.
220
,
3464
-
3477
.