Within a few hours of the naval sonar drill, reports arrived of stranded beaked whales appearing over many kilometres along the coast.  These animals showed signs of decompression sickness, also known as ‘the bends’.

Post-mortems on these animals revealed gas and fat bubbles in their bones and tissues.

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The deeper you dive, the more the pressure forces nitrogen and oxygen from your lungs to dissolve into your body tissues.  If you then surface too quickly, these gases can come out of solution and form bubbles in your blood.  These can block smaller blood capillaries, cutting off the oxygen supply to the affected tissues.  Decompression sickness is a recurrent risk amongst scuba-divers who breathe compressed air, and breath-holding ‘free-divers’ who make too many consecutive dives.

In contrast, beaked whales routinely hunt for an hour below 1000m, using echolocation.  These ‘extreme divers’ do not normally experience decompression sickness, although fossils from early in their evolutionary history show that they were not immune to these problems.  X-rays of the fossilised bones of more primitive whales show regions where bubbles formed inside a capillary, damaging the bone tissue and leaving a tell-tale signature.

Whale embryos initially develop rear limb buds, like land mammals.  These structures are reabsorbed back into the body later in development. The fossil record, along with DNA studies, reveal that whales’ closest living relatives are cows and hippos, which share their same four-legged (tetrapod), hoofed, land-dwelling ancestors.

This raises some puzzling questions:

– Why did whales’ ancestors take to the water after 300 million years on land?

– Why didn’t they re-evolve gills?

– How can they dive for so long without getting ‘the bends’?

Why did whales’ air breathing ancestors take to the water?

The land-dwelling ancestors of whales may have first waded into the sea to escape from predators on land.  Shallow coastal areas offered a relatively safe haven with little competition for the new food resources available in or near the water.  This initial stage would have enabled these semi-aquatic ancestors of modern whales to adapt their digestive systems to a marine food source.

Fossils from the early Eocene (52Ma) show a succession of increasingly aquatic forms.  From crocodile-like and otter -like amphibious hunters, developmental changes remodelled their breathing, senses, kidney function and limbs to survive better in water.  By 40Ma, these early whales had flippers, a fluked tail, and could mate, birth and suckle their young without leaving the water.

At the Eocene-Oligocene boundary (around 36Ma), movement of the continental plates opened up the deep waters of the circum-Antarctic ocean.  This offered new ecological roles for the deeper-diving whales.  Many new whale species appeared, including ancestors of the filter-feeding baleen whales and toothed whales that hunt in deep waters using echolocation.

Why didn’t whales re-evolve gills?

The ability to breathe underwater like fish seems at first like a requirement for life in the sea.  However despite their lack of gills, whales and dolphins are highly effective predators in both shallow and deep water.

Modern whales’ warm bodies enable their fast reflexes for hunting.  Whilst swordfish and tuna have some warm muscles, most of their tissues are at sea water temperature.  Were their whole bodies warm, the heat loss from their gills would be energetically too costly.

Fish gills develop from the ‘branchial arches’; bulging structures in the early vertebrate embryo.  These same tissue bulges give rise to the lower jaw, the middle ear, hyoid bone and larynx in the throat of humans and other mammals.  For whales and other mammals to form gills would require that they develop new embryonic structures; this would render redundant the lungs with their vast area of vascular tissue.

Breathing air enables whales to use vocal signals to coordinate their social groups and attract mates.  Like land mammals, the baleen whales make vocal calls by passing a controlled air flow through the larynx.  Echolocation, the alternative means of producing sound used by dolphins and other toothed whales, also requires air.  Their ‘sonic lips’ generate calls in an air-filled nasal passage.  Whilst many fish make sounds, their vocal abilities are simple and limited.

How do they dive for so long without getting ‘the bends’?

All mammals store oxygen in their muscles using a protein called myoglobin.  Sustained activity during long foraging dives requires a lot of oxygen.  Deep divers have much higher muscle myoglobin concentrations than land mammals, giving them substantial oxygen reserves.

Modern diving mammals, and deep diving fish such as tuna, have also modified their myoglobin.  As early whales began to explore the deeper waters, selection resulted in better survival from individuals whose myoglobin carried a stronger positive electrostatic charge.   Like positive magnetic poles, these ‘supercharged’ molecules repel each other.  This keeps them in solution, allowing them to function at high tissue concentrations where most other proteins would clump together.

A supercharged form and high concentration of myoglobin makes it possible for deep diving mammals to return to the surface slowly after a prolonged dive.  This behaviour avoids decompression sickness.

However when beaked whales and other species encounter naval sonar at depth, this causes them to ‘panic’ and surface too quickly, inducing ‘the bends’.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Balasse M et al. (2006) ‘Stable isotope evidence (δ13C, δ18O) for winter feeding on seaweed by Neolithic sheep of Scotland’ Journal of Zoology 270(1); 170-176

Beatty B L & Rothschild B M (2008)  ‘Decompression syndrome and the evolution of deep diving physiology in the Cetacea’  Naturwissenchaft 95;793-801

Costa D P (2007) Diving physiology of marine vertebrates’ Encyclopedia of life sciences doi:10.1002/9780470015902.a0004230

Ferguson S H et al. (2012) ‘Prey items and predation behavior of killer whales (Orcinus orca) in Nunavut, Canada based on Inuit hunter interviews’  Aquatic Biosystems 8 (3); http://www.aquaticbiosystems.org/content/8/1/3

Gatesy J et al. (2013) ‘A phylogenetic blueprint for a modern whale’  Molecular Phylogenetics and Evolution’ 66:479-506

Mirceta S et al. (2013) ‘Evolution of mammalian diving capacity traced by myoglobin net surface charge’  Science 340;1234192

Nery M F et al. (2013) ‘Accelerated evolutionary rate of the myoglobin gene in long-diving whales’  Journal of Molecular Evolution 76;380-387

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Some 300m below the ocean surface it is always twilight, and cold…  The water is barely above zero.  Fast-moving squid hide here from predatory fish which stay near the surface; at this depth, their nerves would be so slowed by the cold that their eyes could no longer see for them to hunt effectively.

But there are exceptions; a stealthy predator dives into this semi darkness.  Whilst the swordfish’s body temperature matches that of the water, its eyes and brain, crucially, stay toasty warm at around 23⁰C.

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Why do swordfish have warm eyes?

A fish’s body temperature usually matches that of the water, meaning they are ‘cold blooded’ (poikilothermic).  Swordfish nerves, like ours and those of other vertebrates, operate only within narrow temperature limits.  The squid is also ‘cold-blooded’, but their elongated nerve cell axons however, are unusually wide, around 0.5mm diameter, and operate well in the cold, allowing them to maintain their fast movements and escape predators.

A few fish species, however, have evolved methods to generate heat in some of their tissues.  Under the chilly, low light conditions of the deep sea, the warm eyes of the swordfish keep its optical nerve signals rapid.  This allows it to register more visual signals per second than can other vertebrate predators.  This fast image resolution ‘slows down’ apparent time and amplifies details, allowing these stealthy hunters to discern the brief flashes of silver that reveal the fleeting movements of small fish and squid.

This prompts some key evolutionary questions;

– How is the swordfish’s eye heat generated?

– How does the swordfish keep the heat localised to its eyes and brain?

– How does keeping body parts at different temperatures adapt swordfish for survival?

How is the swordfish’s eye heat generated?

Swordfish eye muscles contain many brown-coloured cells that produce heat without shivering (non-shivering thermogenesis).  They have a high metabolism (respiration rate) and contain many of the organelles known as mitochondria.

Mitochondria are formerly free-living bacteria found inside nearly all animal, plant and fungal cells. They ‘breathe’ for their cell, converting sugars and oxygen into carbon dioxide and water.  This releases energy, which they use to pump hydrogen ions (H⁺, protons) from the internal matrix into their inter-membrane space.  They use the chemical energy gradient this creates to produce adenosine triphosphate (ATP), life’s energy storage compound.  These cellular energy factories are found in all animals and plants.

Humans and other mammals have brown adipose cells, also called ‘brown fat’.  The mitochondria in these cells make very little ATP.  Instead, ‘uncoupling proteins’ rearrange negatively charged fatty acids in the mitochondrial inner membranes to face into the inter-membrane space.  These associate with the positively charged protons, then ‘flip-flop’, carrying them back into the matrix and dissipating the energy gradient as heat.

How does the swordfish keep the heat localised to its eyes and brain?

When our bodies generate heat in a cold environment, this sets up an energy gradient; the bigger the differences between our internal and external temperature, the faster we cool.  Warm bodies in a cold environment lose heat quickly, unless insulated.  Birds use feathers, most mammals use fur and whales have blubber.

Fatty insulation over the swordfish’s skull retains heat, and helps keep its eyes and brain at a near constant temperature.  These tissues are homeothermic (maintaining a stable temperature), whilst the rest of its body is poikilothermic (allowing temperatures to vary with the environment).  Blood vessels supplying oxygen to the swordfish’s eye muscles are also arranged to retain heat.  These vessels run in parallel, allowing outgoing veins to warm incoming arteries (this is known as a ‘counter-current’ heat exchange system).

Insulation (fur, feathers or fat), combined with a blood supply arranged to allow counter-current heat exchange, are found in many cold-adapted animals.  Lowering surface temperatures reduces the energy difference between a body and its surroundings, so minimising heat loss.  Warm-bodied migrating species such as wolves and many birds from polar regions use a counter-current exchange to reduce the temperatures of their legs and feet.  This means that their body parts in contact with snow or ice remain at just above zero.

How does keeping body parts at different temperatures adapt swordfish for survival? 

Keeping your body at a different temperature from your environment requires a lot of energy.  The swordfish’s ‘dual temperature’ body isolates the heat and keeps it in one well-insulated region; this is the most energy efficient way for these ‘wait and sprint’ hunters to survive in this environment.  Tuna are another example of a fish with warm and cool tissues.  Their red muscles along their spine are warm, and sustain constant ‘slow’ strokes of the tail during their long distance migrations.

When we sweat, water evaporates and cools our skin surfaces.  Dogs and many other mammals pant to evaporate water from their tongue and mouth cavity.  Elephants lack both sweat glands and a panting reflex; these are possible remnants of their aquatic ancestry.

In very high temperatures they enter a whole-body heterothermic state.  They slow their metabolism, lowering their morning body temperature.  They then absorb daytime heat, raising their temperature above 36.7⁰C, and radiate this ‘stored’ heat at night.

Varying the temperature at times like elephants, or in certain tissues like swordfish, is known as heterothermy.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

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‘It’s head is as long as I am tall!’

       ‘What is it?’

‘Hmm…  A giant fish?  A lizard?  Don’t know.’

       ‘Well I know!  It’s a sea dragon!’ 

It is spring, 1811, the morning after a storm.  Mary is 12 years old, and fearless.  She edges across the cliff to where her brother is already working to free the fossil bones.  Fragments of weathered mudstone clatter down onto the beach.  The eye sockets of the huge skull are wider than the span of her hand.

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During the 200 million years that dinosaurs roamed the land, the oceans were ruled by formerly land-dwelling reptiles.  Of these, ichthyosaurs adopted dolphin-like forms, plesiosaurs became sea lion-like, and mosasaurs occupied crocodile-like ‘ambush’ predator roles.

Of these, ichthyosaurs were arguably the most successful.  Their multiple adaptations to a fully aquatic life included huge eyes, a stiffened, fluked tail, and the ability to mate and give birth to live young in water.  Much as killer whales do today, these predators structured the marine ecosystem.  Many came to resemble the modern whales, dolphins and tuna fish that now fulfil similar ecological roles.  The convergence of body forms between some ichthyosaur species and tuna are particularly astonishing because these reptiles were air breathers.

Why did icthyosaurs evolve to look like modern marine animals?

Life in water poses a specific set of challenges.  These marine reptiles fulfilled similar ecological roles  to whales, and in time evolved body forms similar to these modern mammals.  This is known as convergence.

Like whales and tuna, ichthyosaurs were adapted for long distance energy-efficient swimming.  The respective horizontal and vertical strokes of both ichthyosaur and dolphin tails give an equally powerful ‘lift’ in both directions, propelling these animals forward in a near straight line.

A further example of this convergence is seen in the modern otter.  Unlike the Ichthyosaurs, both whales and otters had land-based mammalian ancestors with a vertically moving spine, giving them their bounding gait.  The whale-like ichthyosaurs moved their tail flukes horizontally, like a modern lizard.

Like whales and tuna, ichthyosaurs were adapted for long distance energy-efficient swimming.  The respective horizontal and vertical strokes of both ichthyosaur and  , propelling these animals forward in a near straight line.

What can modern animals tell us about ichthyosaurs?

Modern tuna and lamnid sharks have converged into a similar ‘deep water sprint-predator’ ecological role.  These long distance migrants move constantly at a moderate speed, except for short fast bursts when chasing prey.  Chunky vertebrae stiffen their bodies at their core, reducing sideways movements except at the narrow ‘hinge’ before the tail.  The continuously active red ‘cruising’ muscles either side of the spine are warm, in marked contrast to most other fish.  In combination with large tendons, these muscles work like pulleys, flicking the fluked tail from side to side. The surrounding white muscles give extra power during short ‘sprints’.

The ichthyosaur Stenopterygius was tuna-shaped with chunky stacked vertebrae.  This stiffened body form suggests that these reptiles converged on the cruise-and-sprint deep water hunting role of modern tuna and lamnids.

Did ichthyosaurs have warm muscles like whales and tuna?

The isotopic proportion between the heavy ¹⁸O and the light ¹⁶O oxygen (the ratio is given as d¹⁸O) in the bones of living fish and marine animals decreases as body temperature increases.  In principle we can use cold-blooded fish fossils as a ‘thermometer’ to indicate the water temperature, and compare this against isotope-predicted body temperatures for other fossil animals from the same rocks.

Oxygen isotope data allows us to infer that Jurassic plesiosaurs and ichthyosaurs had body temperatures of around 35⁰C, much higher than that of their environment.  This indicates that they could generate heat, and may well regulated their body temperatures independently of their environment (homeothermy).  Modern warm bodied marine animals have to conserve their body heat.  This means it is reasonable to infer that ichthyosaurs used similar methods such as a counter-current blood circulation  system and/or heat-insulating blubber.

What happened to the ichthyosaurs?

Ichthyosaurs dominated the world’s oceans for around 150 million years, but then disappeared from the fossil record after the mid-Cretaceous (around 95Ma).  The cause of their sudden extinction remains a mystery.  The empty ecological roles that this created were later filled by mosasaurs; relatives of modern monitor lizards including the Komodo dragon.  In turn these reptiles died out during the Cretaceous-Tertiary mass extinction (65Ma), making way for the later evolution of modern whales, dolphins and tuna.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

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