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

Carey, F.G. (1982)  A brain heater in the swordfish.  Science 216, 1327-1329.

Fritsches, K.A. et al. (2005)  Warm eyes provide superior vision in swordfishes.  Current Biology 15, 55-58.

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Weissenbrock, N.M. et al. (2012)  Taking the heat; thermoregulation in Asian elephants under different climatic conditions.  Journal of Comparative Physiology, B 182, 311-319.

Pausing on the bank, the lead female gathers her herd, ensuring that she is followed before she plunges in. 

The smaller elephants swim, heads fully submerged.  Others walk at first.  All are snorkel-breathing through their trunks. 

A lone male follows at a distance.  He watches the tribe for a moment before he too enters the water.

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Elephants are the largest land mammals, and are at home in hot, dry savannah environments. They migrate hundreds of miles in search of food, and when required will cross rivers, lakes, and even undertake marine excursions.  They are surprisingly strong swimmers, and are the only mammals able to snorkel.

This provides a vital evolutionary clue to their past.  Although we associate elephants with dry land, their bodies reveal clear evidence of an aquatic ancestry.

Fossils and DNA put elephants amongst the swimmers

DNA evidence:

Comparing DNA sequencesenables usto build molecular phylogenies, or ‘family trees’, defining the genetic relatedness between species.  These phylogenies show that elephants’ closest living relatives are the fully aquatic sea cows; the dugongs and manatees.

Fossil evidence:

Water molecules (H₂O) contain three isotopes of oxygen; ¹⁶O, ¹⁷O and ¹⁸O.  The lighter forms evaporate more easily, slightly enriching lakes and oceans with ‘heavy’ water.  This then can become incorporated into aquatic plants and the bodies of animals that graze on them.  Analysing the ratio of ‘light’ ¹⁶O to ‘heavy’ ¹⁸O isotopes (i.e. d¹⁸O) in teeth from fossils of the extinct elephant ancestor Moeritherium, show that they contain a higher proportion of ¹⁸O than teeth from land grazing animals.  This tells us that it ate mostly freshwater plants, suggesting its lifestyle was at least semi-aquatic.

Elephant embryos reveal adaptations to breathing under water

Elephants can snorkel because of their elongated trunks, and elastic connective tissues that fill the space between their lungs and their body wall.  Both of these features appear together early in the foetus, suggesting that they were important for survival of the elephant’s ancestors.

As in other large mammals, elephants’ blood pressure is high; this is needed to keep the brain well supplied with oxygenated blood.  Under water, the differences between the pressure of inhaled air (atmospheric; 0mmHg) and the blood pressure in the capillaries (150mmHg) would be enough to rupture blood vessels and the delicate linings of the lung.  Their elastic connective tissues act as shock absorbers, protecting the lungs against such damage.

Elephants’ testes are inside the body like other aquatic mammals

The location of a mammal’s testes is related to temperature.  Excessive heat or cold will kill mammal sperm (including humans), causing sterility.  Hence in puberty, boys’ testes descend into sacs that are slightly cooler than the interior of their bodies.  However aquatic mammals continue to carry their testes inside their abdomen to protect them from cold.  We would expect land-dwelling elephants’ testes to be carried in a scrotum.  Instead, their testes remain inside the body like those of aquatic mammals.

Early in the foetal development of both male elephants and dugongs, an artery develops which directly connects their kidneys and testes.  In contrast, the testes of most land mammals have a less direct connection, allowing them to descend into a scrotum during puberty.  This suggests that like modern dugongs, the elephants’ ancestors lack a scrotum.

Aquatic mammals including dugongs have a plexus of blood vessels that cool their internal testes and uterus through a counter-current heat exchange  mechanism.  Testicular cooling by a blood plexus has not yet been investigated in elephants; however in the absence of heat stress, they maintain a body temperature of around 34-36⁰C, which is similar to the temperature of the scrotum in most other land mammals.

Elephants ears close for swimming

After swimming we often have to shake our head to clear water from our ears.  However elephant ears have a unique sphincter-like muscle that closes the ear canal and prevents water entry when swimming.  This also creates a sealed ‘acoustic tube’, which works with the aerated bones and ‘acoustic fat’ lenses of the elephant skull to amplify low frequency ‘infrasound’.  Dugongs have similar aerated skull bones and fatty deposits; again implying that they share an aquatic ancestor.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Fowler, M.E. and Mikota, S.K. (eds) (2006) Biology, Medicine, and Surgery of Elephants.  Blackwell.

Gaeth, A.P. et al. (1999)  The developing renal, reproductive and respiratory systems of the African elephant suggest an aquatic ancestry.  Proceedings of the National Academy of Sciences, USA  96, 5555-5558.

Hildebrandt, T. et al. (2007)  Foetal age determination and development in elephants.  Proceedings of the Royal Society of London, B 274, 323-331.

Johnson, D.E. (1978)  The origin of island mammoths and the Quaternary land bridge history of the Northern Channel Islands, California.  Quaternary Research 10, 204-225.

Johnson, D.E. (1980)  Problems in the land vertebrate zoogeography of certain islands and the swimming powers of elephants.  Journal of Biogeography 7, 383-398.

Liu, A.G.S.C. et al. (2008)  Stable isotope evidence for an amphibious phase in early proboscidean evolution.  Proceedings of the National Academy of Sciences,USA 105, 5786-5791.

McKenchie, A.E. and Mzilikazi, N. (2011)  Heterothermy in Afrotropical mammals and birds: a review.  Integrative and Comparative Biology 51, 349-363.

O’Connell-Rodwell, C.E. (2007)  Keeping an ear to the ground: seisemic communication in elephants.  Physiology  22, 287-294.

Poulakakis, N. et al. (2006)  Ancient DNA forces reconsideration of evolutionary history of Mediterranean pygmy elephantids.  Biology Letters 2, 451-454.

Poulakakis, N. and Stamatakis, A. (2010)  Recapitulating the evolution of Afrotheria: 57 genes and rare genomic changes consolidate their history.  Systematics and Biodiversity 8, 395-408.

Seiffert, E.R. (2007)  A new estimate of Afrotherian phylogeny based on simultaneous analysis of genomic, morphological and fossil evidence.  BMC Evolutionary Biology 7, 224.

Springer, M.S. et al. (2004)  Molecules consolidate the placental mammal tree.  Trends in Ecology and Evolution 19, 430-438.

Weissenbrock, N.M. et al. (2012)  Taking the heat: thermoregulation in Asian elephants under different climatic conditions.  Journal of Comparative Physiology, B 182, 311-319.

West, J.B.  Why doesn’t the elephant have a pleural space?  Physiology 17, 47-50.

West, J.B. et al. (2003)  Fetal lung development in the elephant reflects the adaptations required for snorkelling in adult life.  Respiratory Physiology and Neurobiology 138, 325-333.

West, J.B. (2001)  Snorkel breathing in the elephant explains the unique anatomy of its pleura.  Respiration Physiology 126, 1-8.