Coming up for air

01/06/2015 |

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.

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.

We have a diving reflex like other mammals. As the water hits our face, our heart slows and muscles under the skin contract, shunting blood into the centre of our body. Water pressure increases by 1 Atmosphere for every 10m depth. At 2 Atmospheres, the air in our lungs is half its original volume. By 50 metres (5 Atmospheres), gaseous oxygen and nitrogen dissolves into our body tissues, and fluid floods into our lungs. The human free-diving depth record is 214 metres (Image: Wikimedia Commons)

We have a diving reflex like other mammals. As the water hits our face, our heart slows and muscles under the skin contract, shunting blood into the centre of our body. Water pressure increases by 1 Atmosphere for every... more 10m depth. At 2 Atmospheres, the air in our lungs is half its original volume. By 50 metres (5 Atmospheres), gaseous oxygen and nitrogen dissolves into our body tissues, and fluid floods into our lungs. The human free-diving depth record is 214 metres (Image: Wikimedia Commons)

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.

Dolphin embryo (Image: Wikimedia Commons)

The hind limbs of this Spotted Dolphin embryo (Stenella frontalis) are visible as small bumps (limb buds) near the base of the tail.  (Image: Wikimedia Commons)

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?

These North Ronaldsay sheep are descended from an Orkney population farmed here since Neolithic times. They graze along the shoreline, feeding almost exclusively on seaweed. Their rumen stomachs have an adapted bacterial population which enables them to digest marine algae (Image: Wikimedia Commons)

These North Ronaldsay sheep are descended from an Orkney population farmed here since Neolithic times. They graze along the shoreline, feeding almost exclusively on seaweed. Their rumen stomachs have an adapted bacteria... morel population which enables them to digest marine algae (Image: Wikimedia Commons)

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?

A sperm whale (Physeter macrocephalus) begins a dive; Gulf of Mexico. Adaptations for cold, deep waters include insulating blubber, lungs designed to collapse under pressure, and locomotion. The fluked tail is a super-efficient ‘caudal oscillator’; both the up and down strokes generate lift, like a birds’ wing. These and other whale and seal species dive deep both to forage and to escape from killer whale (Orcinus orca) attacks (Image: Wikimedia Commons)

A sperm whale (Physeter macrocephalus) begins a dive; Gulf of Mexico. Adaptations for cold, deep waters include insulating blubber, lungs designed to collapse under pressure, and locomotion. The fluked tail is a super-e... morefficient ‘caudal oscillator’; both the up and down strokes generate lift, like a birds’ wing. These and other whale and seal species dive deep both to forage and to escape from killer whale (Orcinus orca) attacks (Image: Wikimedia Commons)

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’?

This diagram shows how myoglobin forms ‘alpha-helical’ spirals around a ‘haem’ co-factor. Haem’s ring-structure holds an iron atom, carrying an electrostatic charge. This attracts and holds an oxygen molecule (red spheres). As carbon dioxide builds up it dissolves to form carbonic acid. This change of pH, alters the electrostatic balance, prompting myoglobin to release its oxygen. The myoglobin protein’s high positive charge also steadies the pH when cells break down sugars without oxygen and produce lactic acid (Image: Wikimedia Commons)

This diagram shows how myoglobin forms ‘alpha-helical’ spirals around a ‘haem’ co-factor. Haem’s ring-structure holds an iron atom, carrying an electrostatic charge. This attracts and holds an oxygen molecule ... more(red spheres). As carbon dioxide builds up it dissolves to form carbonic acid. This change of pH, alters the electrostatic balance, prompting myoglobin to release its oxygen. The myoglobin protein’s high positive charge also steadies the pH when cells break down sugars without oxygen and produce lactic acid (Image: Wikimedia Commons)

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
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Bats; hunters that see in sound

07/08/2014 |

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.

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.

A bottlenose dolphin (Tursiops truncatus) with locator beacon; Persian gulf. This animal is part of a trained team of animals used by the US Navy for mine clearance in shipping lanes. Since most prey cannot detect high frequency sound, hunters using echolocation have a stealth surveillance system of near-military precision. Dolphin echolocation inspired naval underwater surveillance using sonar (Image: Wikimedia Commons)

A bottlenose dolphin (Tursiops truncatus) with locator beacon; Persian gulf. This animal is part of a trained team of animals used by the US Navy for mine clearance in shipping lanes. Since most prey cannot detect high ... morefrequency sound, hunters using echolocation have a stealth surveillance system of near-military precision. Dolphin echolocation inspired naval underwater surveillance using sonar (Image: Wikimedia Commons)

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.

Bats and other echolocators emit pulses of directional sound that echo back from a target, returning them a cone of sonic information. They control the length and width of this cone by altering the frequency of their calls and how far they open their mouths when producing the pulse. Larger mouths and higher frequencies produce longer, narrower ‘visual’ sound cones (Image: ©Simon Crowhurst)

Bats and other echolocators emit pulses of directional sound that echo back from a target, returning them a cone of sonic information. They control the length and width of this cone by altering the frequency of their ca... morells and how far they open their mouths when producing the pulse. Larger mouths and higher frequencies produce longer, narrower ‘visual’ sound cones (Image: ©Simon Crowhurst)

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.

 

The human eye shifts its main focus in a series of ‘saccade and fixate’ movements. As this eye focusses on Sophocles’ hand, reflected light from the object lands on the fovea; the detail-harvesting area at the back of the eye. When looking at an object, our eyes move suddenly from one detail to another (the saccade), and then ‘fixate’ for a few moments onto these points of interest. Sophocles uses the idea of blindness in his story, ‘Oedipus Rex’, to illustrate how seeing is a highly active process, whether this is physical or metaphorical (Image: Composite of images from Wikimedia Commons)

The human eye shifts its main focus in a series of ‘saccade and fixate’ movements. As this eye focusses on Sophocles’ hand, reflected light from the object lands on the fovea; the detail-harvesting area at the bac... morek of the eye. When looking at an object, our eyes move suddenly from one detail to another (the saccade), and then ‘fixate’ for a few moments onto these points of interest.Sophocles uses the idea of blindness in his story, ‘Oedipus Rex’, to illustrate how seeing is a highly active process, whether this is physical or metaphorical (Image: Composite of images from Wikimedia Commons)

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.

 

This artist’s impression shows the flight path (below) and behaviour (above) during the hunting sequence of a Common Pipistrelle bat (Pipistrellus pipistrellus), represented by the sound trace (centre). The process has distinct phases. During the initial ‘search’ (left), the call frequency is less frequent and at lower amplitude; this produces a wide angle sound cone. As it scans the environment, the bat turns its head from side to side. Upon detecting a target (centre), the hunter makes an ‘approach’; here the calls increase in volume and frequency, which focusses the acoustic gaze. In the third phase (right), the hunter is locked onto its target, and produces a high frequency ‘buzz’. This provides a highly detailed focussed cone of sound, allowing the bat to manoeuvre very precisely as it closes in and takes the prey. From the start of the approach to reaching the target takes less than a second (Image: ©Simon Crowhurst). Listen to the sounds represented above, modulated into our hearing range by a ‘bat detector’. Watch how the sound direction becomes more targeted as a hunting bat (circle) locks onto and captures a flying insect (cross).

This artist’s impression shows the flight path (below) and behaviour (above) during the hunting sequence of a Common Pipistrelle bat (Pipistrellus pipistrellus), represented by the sound trace (centre). The process ha... mores distinct phases. During the initial ‘search’ (left), the call frequency is quieter (lower amplitude) and less frequent; this produces a wide angle sound cone.  Upon detecting and approaching a target (centre), the hunter’s calls increase in volume and frequency, which focusses the acoustic gaze.  As the hunter is locked onto its target (right), it produces a high frequency ‘buzz’. This highly focussed cone of sound allows the bat to perceive details, and manoeuvre very precisely as it closes in to take the prey.The time from detecting to taking the prey is less than a second.  (Image: ©Simon Crowhurst)

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.

The Allen Telescope Array (ATA) built by the University of California, Berkeley and SETI (Search for Extra-terrestrial Intelligence). This offset Gregorian design reflects incoming radio waves caught by the large parabolic dish onto the secondary parabolic reflector, which harvests the signal. The telescope is tuned to a frequency range from 0.5 to 11.2 GHz and will eventually have 350 antennae (Image: Wikimedia Commons)

The Allen Telescope Array (ATA) built by the University of California, Berkeley and SETI (Search for Extra-terrestrial Intelligence). This offset Gregorian design reflects incoming radio waves caught by the large parabo... morelic dish onto the secondary parabolic reflector, which harvests the signal. The telescope is tuned to a frequency range from 0.5 to 11.2 GHz and will eventually have 350 antennae (Image: Wikimedia Commons)

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.
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