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

Noren S R et al. (2012) ‘Changes in partial pressures of respiratory gases during submerged voluntary breath hold across odontocetes; is body mass important?’  Journal of Comparative Physiology B 182;299-309

Orpin C G et al. (1985) ‘The rumen microbiology of seaweed digestion in Orkney sheep’  Journal of Microbiology 58(6); 585-596

Rothschild B M et al (2012) ‘Adaptations for marine habitat and the effect of Jurassic and Triassic predator pressure on development of decompression syndrome in ichthyosaurs’  Naturwissenchaften 99;443-448

Steeman M E et al. (2009) ‘Radiation of extant cetaceans driven by restructuring the oceans’  systematic biology 58;573-585

Thewissen J G M et al (2007) ‘Whales originated from aquatic artiodactyls in the eocene epoch of India’  Nature 450;1190-1195

Thewissen J G M et al (2006) ‘Developmental basis for hind-limb loss in dolphins and origin of the cetacean body plan’ Proceedings of the National Academy of Sciences USA 103(22); 8414–8418

Thewissen J G M and Sunil B (2001) ‘Whale origins as a poster child for macroevolution’  Bioscience 51(12);1037-1049

Tyack P L (2006) ‘Extreme diving of beaked whales’  Journal of Experimental Biology 209;4238-4253 Naturwissenchaften 99:443-448

Uhen M D (2010) ‘The origin(s) of whales’  Annual Review of Earth and Planetary Sciences 38;189-219

Uhen M D (2007) ‘Evolution of marine mammals; back to the sea after 300 million years’  The Anatomical Record 290;514-522

Williams T M (1999) ‘The evolution of cost efficient swimming in marine mammals; limits to energetic potimization’  Philosohical Transactions of the Royal Society of London series B  354;193-201

You are out in the dark, alone.  You become aware of a distant rhythmical clicking noise.  Sensing danger, you change direction and head for cover.  Seconds later you are punched by wave after wave of sound that hits your body like a machine gun.  The noise bears down on you, loud as an aircraft, faster and faster, blurring into a roar…. 

    …You are a moth, taken by an echolocating bat.

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Bats aren’t blind.  Their eyes work, but they live in a different world, requiring an extra sense.  Using high frequency sounds, also known as ‘biosonar’ or ‘echolocation’, they can see in the dark.  We see, hear touch, smell and taste by picking up cues in our environment.  Biosonar is completely different; there can be no signal without the call.

This really is seeing in sound.  Biosonar provides bats and some other animals, including dolphins, with a distinctive and sophisticated form of vision, giving detailed three-dimensional information over long distances in darkness or murky waters.

Bats illuminate their world with beams of directional sound

Most bats hunt using a range of frequencies, moving their heads to pulse sounds in different directions as they fly.  Lower frequencies produce wider sound cones like a floodlight, and higher frequencies focus the beam like a spotlight.

Although one lives in the forest and the other in the ocean, the way bats and dolphins use biosonar when hunting is almost identical.  Dolphins, like bats, both shift the frequency of their clicks as they scan and lock onto prey, giving a characteristic ‘buzz’ of rapid calls as they take the target.  Sound travels more quickly under water, so dolphin sonar operates over a longer range.

Bats project sound and receive echoes the way that eyes scan an image

Watch someone’s eyes as they examine something; their gaze jerks from one area to another.  These are known as ‘saccade and fixate’ movements.  They focus different parts of the image onto an area at the back of the eye called the fovea, which sees detail.  ‘Saccade and fixate’ eye patterns are found in all animals with good vision, and is a defining characteristic for how eyes focus on details.

 

When our eyes focus, they project an image onto an area at the back of our eyes known as the ‘fovea’.  This zone is specialised to pick up high levels of detail.  Any sense can be developed to pick up a high level of detail; we use sight, bats use sound, and star-nosed moles use touch.

Most bats hunt insects in the open air, listening for the returning echoes before making their next signal.  They use a combination of head movements and focussed sound cones to gain information in a classic ‘saccade and fixate’ pattern.  Wider head scanning and lower frequency calls provide a ‘wide angle’ view with less detail.  Higher frequency calls and a narrow range of head movements create an ‘acoustic fovea’; this focuses their sonic gaze onto a small area and recovers detail, much like ‘zooming in’ using a macro lens.

 

Horseshoe bats use echolocation in a different way; an adaptation to hunting in and around the spatially variable (and hence acoustically complicated) ‘surface’ of tree and shrub canopies.  They use mostly constant-frequency pulses, and listen for Doppler-shifted returning echoes.  The cochlear membranes of their inner ears respond over a broad frequency range, but have particular sensitivity within a very narrow bandwidth (their acoustic fovea).  When locking the sound pulse onto their prey, they alter their emitted call in order to keep the frequency of the returning echoes constant.  This allows them to focus on the frequency modulations caused by the fluttering movements of large insects.

 Echolocation reveals shape and form using ‘stereo’ images

Just as the brain uses the different view from our two eyes to build a stereo image, our brains use the differences between what is heard by our ears to understand something of the direction and distance of a sound source.  Bats use this difference to understand and construct a ‘stereo image’ of their surroundings in three dimensions.  This enables them to understand something of the shapes and textures of objects in their environment.

Some tropical bats are nectar feeders.  Flowers hidden amongst the leaves are in an acoustically cluttered environment.  Many flowering plants using bats to assist with their pollination have evolved floral structures that act as ‘sound beacons’.  These are usually dish-shaped (parabolic) and bounce back an unique echo pattern that makes them become acoustically visible.

Parabolic shapes also make excellent receivers.  The Search for Extra-Terrestrial Intelligence (SETI) project’s radio telescope is made of many parabolic ‘ears’, listening for radio transmissions from outer space.  Whilst we have invented technologies enabling us to hear bat calls and signals from beyond our planet, our own ears’ convoluted parabolic shape also captures sounds, and funnels them to our receiver; the ‘ear drum’ .

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Fenton, M.B. (2013)  Questions, ideas and tools; lessons from bat echolocation.  Animal Behaviour 85, 869-879.

Connor, W.E. and Corcoran, A. J. (2012)  Sound strategies; the 65 million year old battle between bats and insects.  Annual Review of Entomology 57, 21-39.

Ghose, K. et al. (2006)  Echolocating bats use a nearly time-optimal strategy to intercept prey.  PLoS Biology 4, 865-873.

Jakobsen, L. et al. (2013)  Convergent acoustic field of view in echolocating bats.  Nature 493, 93-96.

Land, M.F. (2011)  Oculomotor behaviour in vertebrates and invertebrates In  The Oxford Handbook of Eye Movements(S.P.Liversedge, I.D. Gilchrist and S. Everling, eds), pp. 3-15. Oxford University Press.

Ratcliffe J A et al. (2012) ‘How the bat got its buzz’  Biology Letters 9;20121031

Siebert, A M et al (2013) ‘Scanning behaviour in echolocating common pipistrelle bats (Pilistrellus pipistrellus) Plos One 8(4);e60752

Simon et al (2011) ‘Floral acoustics; conspicuous echoes of a disc-caped leaf attract bat pollinators’  Science 333: pp631-633

Schnitzler, H-U. and Denzinger, A. (2011)  Auditory fovea and doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals.  Journal of Comparative Physiology, A 197, 541-559.

Surlykke, A. et al. (2009)  Echolocating bats emit a highly directional sonar sound beam in the field.  Proceedings of the Royal Society of London, B 276, 853-860.

von Helversen, D. and von Helversen, O. (2003)  Object recognition by echolocation; a nectar feeding bat exploiting the flowers of a rainforest vine.  Journal of Comparative Physiology, A 189, 327-336.

von Helversen, D. and von Helversen, O. (1999)  Acoustic guide in bat pollinated flower.  Nature 398, 759-760.

Early whaling logs often referred to whales as ‘singers’.  All whales use sounds for communication, and most use recognisable patterns, ranging from the haunting tones of bowhead whales to the fast echolocation.  Bowheads and bottle nosed dolphins use ‘names’ to identify each other and their clan, have ‘conversations’, and copy each other’s calls.

Bowheads are second only in size to the blue whale, and are very long-lived. Stone harpoon heads, which went out of use at the turn of the 19th century, have been found lodged in the bodies of some individuals of today.  Listen to their calls here.

Whales’ land-based ancestors made sounds as we do, using the throat and mouth.  But try singing under water!  Whales call during dives; whilst holding their breath, and with their mouths closed.  Calling is essential for these highly social animals; this is evident because independently both baleen and toothed whales have evolved new ways to produce and transmit sound in the sea.

How are whale sounds made?

We produce sound in a tubular organ in our throats; the larynx.  This organ is an air valve, closing off the lungs when we swallow, and controlling the outward flow of air.  Sound is generated by vibrating paired membranes in the larynx; these ‘chop up’ the airflow into pressure waves.  This is then modified by resonating in the chambers of the chest, nose and throat before being released through the mouth.

A humpback’s larynx does not sit across the windpipe.  Instead it straddles the opening to an additional air sac located beneath the throat.  These whales make sounds by passing air between this sac and the windpipe, vibrating the vocal folds of the larynx.  These deep notes are modified and amplified by resonating in the laryngeal sac and nasal cavity, and are thought to be transmitted into the water through the sac, which vibrates the flexible throat pleats somewhat like a hi-fi speaker cone.

Dolphins have evolved a secondary set of vocal folds inside their nasal cavities, called ‘phonic lips’.  These vibrate like our vocal chords and generating pressure waves.

Because during deep dives the air volume in their nasal cavities becomes very small, their clicks, rasps and whistles do not resonate in inner cavities.  Instead, a lens of fatty material on the front of the skull known as the ‘melon’ acts as an underwater ‘speaker cone’, amplifying and transmitting these calls.

Why do whales ‘sing’?

The repetitive, phrased songs of humpback whales are a means of male display.  Whilst both genders make sounds, only the males produce song patterns.  They copy the signature calls of their clan, serenading unaccompanied females during seasonal migration  and at the winter breeding grounds.

Their behaviour suggests that these breeding areas are a form of ‘floating lek’, where females ‘browse’ amongst available mates. Humpbacks also use other non-singing signals, e.g. when hunting together, females call to communicate with their offspring.

Bottle-nosed dolphins develop their own distinctive signature whistle in the first few months, and exchange these ‘names’ when meeting other dolphins.  Females keep their whistle throughout life, whilst males change their signature calls when they move between social groups. Like baleen whales, they also communicate during foraging dives and to maintain social ties.

What can we learn from whale song?

Biologists classify ‘song’ as following ‘a repeating, predictable acoustic pattern’.  Most songbirds mimic the calls of their peer group  as juveniles.  When they mature, this song pattern becomes ‘fixed’.  Whales are unusual; they can copy and learn new sounds throughout their lives.  Like us, they have a brain structure that continuously learns and can adapt to changes.

The diversity of signature calls and unique song patterns used by clans reveal that whales have a complex and sophisticated system of learnable language.  Studying the language and culture of whale populations can thus provide clues about how own language and social complexity may have evolved.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Adam O et al. (2013) ‘New acoustic  model for humpback whale sound production’  Applied Acoustics 74: 1182-1190

Cantor M and Whitehead H (2013) ‘The interplay between social networks and culture; theoretically and among whales and dolphins’  Philosophical Transactions of the Royal Society B 368: 20120340

Cholewiak D M (2013) ‘Humpback whale song hierarchicial structure; historical context and discussion of current classification issues’  Marine Mammal Science 29 3: E312-E332

Cranford, T.W., (2000)  "In Search of Impulse Sound Sources in Odontocetes." In Hearing by Whales and Dolphins (Springer Handbook of Auditory Research series), W.W.L. Au, A.N. Popper and R.R. Fay, Eds. Springer-Verlag, New York.

Fitzgerald EMG (2006) ‘A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales’  Philosophical Transactions of the Royal Society B 273:2995-2963

Green SR et al. (2011) ‘Recurring patterns in the songs of humpback whales (Megaptera novaeangeliae)’  Behavioural Processes 86:284-294

Janik VK (2005) ‘Acoustic communication networks in marine mammals’  pp390-415 in Animal Communication Networks  McGregor PK (Ed) CUP, Cambridge

Janik VK (2009) ‘Whale song’ Current Biology  19(3)R9-R11

Jensen FH et al. (2011)  ‘Calling under pressure; short finned pilot whales make social calls during deep foraging dives’  Philosophical Transactions of the Royal Society B 278:3017-3025

King S L et al. (2013) ‘Vocal copying of individually distinctive signature whilstles in bottlenose dolphins’  Philosophical Transactions of the Royal Society B 280:20130053

Madsen PT et al (2002) ‘Sperm whale sound production studied with ultrasound time/depth-recording tags’  Journal of Experimental Biology 205: 1899-1906

Madsen P T et al. (2002) ‘Male sperm whale (Physeter macrocephalus) acoustics in a high latitude habitat: implications for echolocation and communication’  Behavioural Ecology and Sociobiology 53:31-41

Madsen PT et al (2012) ‘Dolphin whistles; a functional misnomer revealed by heliox breathing’  Biology Letters 8: 211-213

Mercado E and Handel S (2012) ‘Understanding the structure if humpback whale songs’ Journal of the Acoustics Society of America 132(5):2947-2950

Mercado E et al.  (2010) ‘Sound production by singing humpback whales’  Journal of the Acoustics Society of America  127(4) 2678-2691     ***NB  I am using the broader definition of ‘song’ as applied here by these authors.  Janik (2009) suggests that only baleen whales are singers because of their more elaborated song patterns.  However toothed whales also use patterns, even though they are clicks and whistles rather than resonating songs.

Møhl B (1999) ‘Dolphin hearing; relative sensitivity as a function point of application of a contact sound source in the jaw and head region’  Journal of the Acoustics Society of America 105(6); 3421-3424

Quick NJ and Janik VM (2012) ‘Bottlenose dolphins exchanges signature whistles when meeting at sea’  Philosophical Transactions of the Royal Society B 279:2539-2545

Reidenberg JS and Laitman JT (2007) ‘Discovery of a low frequency sound source in Musticetae (baleen whales); anatomical establishment of a vocal fold homologue’  Anatomical Record 290: 745-759

Reidenberg JS and Laitman JT (2008)  ‘Sisters of the sinuses; cetacean air sacs’  Anatomical Record 291:1389-1396

Smith J N et al (2008) ‘Songs of humpback whales, Megaptera novaengeliae, are involved in intersexual interactions’  Animal Behaviour 76:467-477

Stafford KM (2012) ‘Spitzbergen’s endangered bowhead whales sing through the polar night’  Endangered Species Research 18:95-103