Why and how does an ‘annual’ chameleon die?

Laborde's Chameleon
Furcifer labordi
Christopher Raxworthy / Public domain

Twelve years ago came the news from Madagascar of an ‘annual’ chameleon—one that spent more time in the egg than as an adult.

In short, Laborde’s Chameleon, Furcifer labordi, was found to grow rapidly after hatching in November, to reach sexual maturity and breed by January-February and then to senesce and die. The adult lifespan was found to be 4-5 months. For the dry season of April to October there were no adults alive, just the eggs remained waiting to hatch at the start of the wet season in November.

The discovery excited a great deal of interest for all sorts of reasons. Not least was that among those studying the phenomenon and mechanisms of ageing, comparative life histories and longevity. Laborde’s Chameleon joined a few species of marsupials amongst tetrapods known to have a short lifespan and to die after a first breeding.

This is not the place to describe the large and controversial field of ageing. However, some of those involved may have been tempted to speculate that these short-lived chameleons might be exemplars of one theory of ageing which contends—erroneously in my view—that organisms have a built-in programme that, around a certain age, leads to death. However, what played on my mind, having once known a bit but never enough about chameleons, was what caused the chameleons to die after reproducing. Would they, for example, live longer if breeding did not take place? Was there something about the environment, a lack of food for example, that prevented their survival as adults?

A clue that Laborde’s Chameleon is not always strictly ‘annual’ came from a different location. Kirindy, where the warm, wet season is longer. There, females were found which had bred more than once and one survived into a second year after a particularly long rainy season. When these chameleons were kept in cages in the same region, some males were found to survive until the next season.

Still, I contend, the best way of looking at differences in lifespan between species is the Disposable Soma Hypothesis of Tom Kirkwood. In essence, because the availability of nutrients within the body is limited, animals balance the amount invested in reproduction and in repair. At one extreme, with Laborde’s Chameleon being an exemplar, the animal goes for rapid growth and reproduction at the expense of essential repairs to its cells, to its DNA, to fighting infection and infestation, to healing its wounds etc; as a result it dies when relatively young. At the other extreme, the slow-growing, slowly reproducing animal invests in keeping the adult in good condition for much longer; as a result it does not fall victim to tumours caused by errors in DNA copying or to infection and thus may live for a very long time; think elephant.

Thus, one might expect, with its defences down, Laborde’s Chameleon to fall victim to something in the environment that a longer-lived species which lives in the same habitat (like the Warty Chameleon, F. verrucosus, which aestivates during the dry season) would be expected to see off. I suggested some time ago to people in conversation that one of the factors that might be involved in the death of short-lived chameleons might be parasites. The reason I argued thus was that I had seen the incredible parasite loads of other species of chameleon after a short time in captivity: worms, protozoans and coccidial spores abounded. I was about to write this article when I came across a paper published in 2019 which examined that very idea—that a low resistance to parasites in Laborde’s Chameleon is what is the proximate cause of death of the adults.

The German group who reported the work from Kirindy joined forces with veterinary colleagues. They found that the parasite load in the alimentary canal increased dramatically during the last three months of life. Males had a greater parasite load internally and externally than females. Some animals were kept in cages—again in their habitat in Madagascar. Those individuals had a lower parasite burden and lived longer than their counterparts living in the wild. The authors concluded that the increased prevalence of gastrointestinal and blood parasites is entirely compatible with less investment in the immune system of these fast-growing, fast reproducing lizards—just as would be predicted from a trade-off between a rapid lifestyle and internal defence and repair.

Males might have been expected to be less affected than females producing eggs. However, it seems that males also put everything into reproduction. There is intense rivalry and bloody combat during the short breeding season as males guard their mates.

The indication of lower parasite loads in, and longer lifespan of, Laborde’s Chameleons kept in captivity in Madagascar suggests the need for further experiments. The animals were fed on invertebrates caught in the wild, some of which would presumably contain parasites. What would happen if, say, newly-hatched individuals were fed on parasite-free livefood? What would be their lifespan and what would they die of?

Finally, this article started off as one about a remarkable chameleon from a remarkable island fauna but it has to end as one about parasites and co-evolution with their hosts. In general, parasites evolve so as to be less lethal to their hosts. They have their own trade-off between going for growth and reproduction and killing the host by taking too much food and causing physical damage. So has co-evolution delivered a suite of parasites that like the chameleon itself go for broke and then in vast numbers lurk in an intermediate species for the onset of the next rainy season?

…and really finally. We did not see Laborde’s Chameleon when we were in southwest Madagascar in 2003. When I realised that was in October I now see why—the eggs were in the ground ready to start hatching in November.

Eckhardt F, Kappeler PM. Kraus C. 2017. Highly variable lifespan in an annual reptile, Labord’s chameleon (Furcifer labordi). Scientific Reports 7: 11397 doi:10.1038/s41598-017-11701-3 

Eckhardt F, Strube C, Mathes KA, Mutschmann F, Thiesler H, Kraus C, Kappeler PM. 2019.  Parasite burden in a short-lived chameleon, Furcifer labordi. International Journal for Parasitology: Parasites and Wildlife 10, 231-240. https://doi.org/10.1016/j.ijppaw.2019.09.010 

Karsten KB, Andriamandimbiarisoa LN, Fox SF, Raxworthy CJ. 2008. Proceedings of the National Academy of Sciences of the USA 105, 8980-8984. doi􏰊10.1073􏰊pnas.0802468105 

How Chameleons Work: Great discoveries in the 1930s by Alexander Zoond aka Alexander or Alec Sand (1901-1945)

SPLAT. KERPOW. The words of a schoolboy comic hardly do justice to the chameleon launching its tongue to capture its prey. That whole process, from moving the eyes into stereoscopic mode, preparing the tongue for launch, the explosion of the tongue from the mouth, to the prey being dragged into the mouth and chewed must surely rank as one of the great sights in the living world. Equally the colour-changing abilities of these lizards has to be seen in real time to be appreciated.

Sadly, and the story even ends on a very sad note, the name of the man who made the most important discoveries in how the chameleon tongue works and of how colour changes are controlled has been largely forgotten. Partly, this is because he changed his name and partly it is because he died young and in tragic circumstances.

The name of the author that appears in list of references to the work on chameleons in the early 1930s is A. Zoond. The only reason I knew that he changed his name is that ETB Francis told me so; he did that while we were talking about his work on chameleons I had supplied him with. Zoond, he said, changed his name to Sand. In fact both names appeared on the extensive reading list ETBF handed out to honours zoology students for his course on vertebrates, a list so extensive a modern student would have an apoplexy, a. from shock over the quantity, and b., from having to work out whole fields of research for themselves.

Alexander Sand
In the tropical, white, uniform of a
Lieutenant, R.N.V.R.
Photograph used in his Royal Society
Obituary Notice

Alexander Zoond or Alexander Sand and, sometimes, Alec Sand is one of my scientific heroes from the then new world of experimental biology. He is sometimes labelled as a comparative physiologists but what he did was excellent physiology; there is nothing to be gained by adding ‘comparative’ or demeaning its fundamental importance because it was not done on mammals. Only fairly recently have I got to know more about him and only last week discovered his tragic end.

Information on him comes mainly from his obituary notice for the Royal Society and a family tree (without much detail) on ancestry.com. F. S. Russell FRS (later Sir Frederick) wrote that Sand was ‘of Jewish-Russian extraction’ and was born in Warsaw on 28 December 1901. The unrest in Poland (his father was a Menshevik) saw the arrival of the family in London when Alec was six. Before Zoond the family name had been Zundelevich or, in South Africa, Zoondevitch.

His schooling in London was entirely on the arts side. After a year at Reading university college came a strange and unexplained move. Reading then was the place for degrees in agriculture but Zoond left for the University of British Columbia in Canada to study dairy bacteriology with the intention of a farming career. After graduating with an agriculture degree, he tried a job in farming in the U.S.A. for a year but found it unrewarding. In 1924 he headed back to Canada, this time to McGill University, for an MSc in bacteriology (his thesis from October 1925, The influence of green manures upon the growth and physiological efficiency of Azotobacter chroococcum, can be found in full online). Appointed to a Demonstratorship in 1926 he had a chance meeting with Lancelot Hogben FRS who was then Assistant Professor of Medical Zoology. Hogben was only at McGill for 18 months and when he was offered the chair of zoology at the University of Cape Town, he took it. With him went Zoond, having turned down a fellowship at Yale, as lecturer.

Lancelot Hogben
Photograph used in his Royal Society
Biographical Memoir

Zoond, in other words, changed field entirely, an attitude entirely in keeping with Hogben’s iconoclasm and loathing of classical zoology and classical zoologists. Hogben wrote:

…I must here explain that the sacred cow of first-year biology in those days was a whimsy of Thomas Henry Huxley known to posterity as the “type system”. This involved the detailed anatomical study of about a dozen species chosen from different groups of the Animal Kingdom, less because they were typical of their phyla or classes than because it was at one time relatively easy to place orders for them with pet shop dealers in London. When I entered my department on the day after arrival, I found the shelves lined with dozens of bottles of Huxleyan types imported in formalin from the seat of the empire. On enquiry, I learned that no living creatures had ever desecrated these hallowed precincts. The same day, I therefore instructed my laboratory steward to empty all the contents of the pickle jars in the yard behind the laboratory ready for the incinerator when the sun had dried them. Henceforth, the motto was to be only the living pass these portals…

Zoond clearly thrived in Cape Town. He published with Hogben on the pH of surface water, with David Slome¹ on the effect of electrolytes on cardiac rhythm and with Enid Charles, (the first wife of Hogben) on respiration in crabs.

In his memoir Hogben did not mention Zoond by name. However, it is clear who is being referred to in the following passage:

When I was not dealing face to face with the student body, Boer-backlashed mentality could make matters disagreeable. The lecturer whom I imported from McGill to replace the relict of my predecessor formed an attachment to one of the only two coloured medical graduates then practising in the Dominion, the other one being her brother-in-law, a leading light in the Moslem Community. Both held the Glasgow degree. When our young colleague confided in us that he was bringing his lady-friend to the University annual dance, both Enid and I scented embarrassment for both. Accordingly, we asked the pair to dine with us so that the lady could come as our own guest. My Jewish students clustered round and saw to it that she was never without a partner. Next day, the more rabid nationalist students held an open air campus meeting of protest.

It was after Hogben, with apartheid in the offing, had left Cape Town in 1930 that Zoond, who had stayed on, completed his work on chameleons, that on the tongue with Joyce Eyre², that on pigmentation with Eyre and with Naomi Adeline Helen Bokenham (later Millard) (1914-1997). The papers were published between 1933 and 1935, as he was leaving or after he had left South Africa.

Cape Dwarf Chameleon (Bradypodion pumilum, in the 1930s known as
Lophosaura pumila and then Microsaura pumila).
All of Zoond's (Sand's) research was on this species.
Photo: JonRicfield from here.

Sand (still Zoond then) left Cape Town in 1933; before doing so he took a Ph.D. from that university. He then went to Cambridge to work with James Gray FRS (later Sir James) then Reader in Experimental Zoology who was just beginning his famous work on animal locomotion. It was their joint work on the locomotory rhythm of the dogfish published in 1936 that was on ETBF’s reading list.

Alexander Zoond changed his name by deed poll on 9 March 1935 to Alexander Sand. The notice in the London Gazette gave his address as 9 Storey’s Way, Cambridge, his occupation as ‘biologist’ and stated that he was a naturalised British subject. I have not been able to work out in what capacity Sand was working with Gray. His second, this time Cambridge, Ph.D. was awarded in 1938. He must have been in statu pupillari to have been awarded a Ph.D. since those paid by the university were (and I think still are) disbarred. Did he have some form of external fellowship or did he fund himself?

In early 1935 he joined the staff of the Marine Biological Association’s famous laboratory at Plymouth as Physiologist. There he worked on the sensory physiology of fish including the lateral line, stretch receptors in the muscles and the ampullae of Lorenzini. The research on the auditory labyrinth he did with Otto Löwenstein (1906-1999, FRS 1955) was—and still is—of relevance in all vertebrates and clinical conditions. What happens in the semicircular canals during movement of the head was sorted out for the first time in experiments that would have been impossible in mammals.

Although I am not going to describe here the work on sense organs in fish, I thought it worth quoting the following paragraph that indicates the sensitivity of the lateral line and why Sand worked in the cellar of the Plymouth laboratory ‘which is hewn out of solid Devonian limestone’:

To demonstrate the delicacy of the response he formed a light hammer of a rubber stopper which was allowed to fall through a distance of 8 cm. on to a rubber sponge lying on the edge of the table about 3 feet away from the prepara­tion, the shocks imparted to the table being quite imperceptible to the human touch. 

There are a few traces in the newspapers of Sand’s time at Plymouth. The Western Morning News of 28 December 1936 reported that a fire had been discovered in Fardel Manor on the Cornwood-Ivybridge road which was occupied by Sand at the time. Large beams underneath a hearth in one of the upstairs rooms were smouldering. One of Sand’s children was due to sleep in the room. The fire brigade had to cut away the floorboards before extinguishing the fire ‘with the aid of patent extinguishers’. The medieval house, now Grade I listed and about 9 miles from the MBA laboratory, was once the seat of the Raleigh family.

By the time of the special census in 1939, the Sand family had moved a couple of miles to Gerston, Harford, now part of Ivybridge. Sand is shown there (as a research biologist) with his wife, Edith G Sand (born 19 April 1909), two children (records still closed) and Elizabeth B Reidy, born 1914, described as ‘paid companion help’. Russell wrote that he had two sons.

Motorists in Britain lived for decades in fear and dread of leaving their car without lights at night. Bored policemen pounding their beats were always on the lookout. Sand was fined ten shillings (50p) at Totnes Petty Sessions for ‘leaving a motor car without lights’ at Redworth Terrace, Totnes on 7 January 1940. How being fined for leaving a car without lights tied in with the wartime blackout regulations which demanded no lights, I do not know. Normal for Devon, maybe.

Russell then notes that Sand did all he could to get into the armed forces as quickly as possible after the outbreak of war.  He was commissioned on 1 May 1940 in Special Branch of the Royal Navy Volunteer Reserve. Promotion to Lieutenant followed in October 1940. He, like many biologists in the war, was involved in radar. Russell wrote:

After a time on the mainland in the north of Scotland he was posted as Officer in Charge of the station on the Shetlands. In 1941 Sand came south to lecture on radar for some months before being posted to a cruiser in which he was in the Indian Ocean. He contracted malaria in the Persian Gulf and when recovered went on leave to South Africa where his wife and two sons were living for the war years. He was then posted to a monitor and was present at the Sicilian and Salerno landings, his ship being hit. After a period of unemployment he was seconded for research at the Naval Department in the Medical Research Council’s Laboratory at Hampstead.

Russell went on to say that the research at Hampstead was on the physiology of diving and that in the course of his duties he received training in diving himself. It was, said, Russell, likely to remain confidential. G. L. Brown (FRS 1946, knighted 1957) was in charge of the research. The Physiological Society always maintained the tradition of using just initials and surnames in its internal communications, never honours or titles, so Sir George Lindor Brown FRS was always G.L. Brown. His biographical memoir contains more details of the research and includes Sand, along with a while string of well-known physiologists and naval officers, as members of the laboratory:

Brown discovered at the Lister Institute, and commandeered, the long-disused chamber that J. S. Haldane, the father of J. B. S., had used a generation earlier in the research that gave divers their first reliable decom­pression tables. The chamber was transported to the garden of the Institute at Hampstead, a hut was built around it, a new compressor was installed, and Brown and his associates began to acquire the somewhat esoteric expertise needed for doing human experiments under pressure. It was Brown’s first opportunity to recruit a research team of his own. H. P. Marks, Macintosh and Collison of the Hampstead staff were already available; they were joined by F. Dickens, C. B. B. Downman and 20-year-old H. B. Barlow; A. Sand and W. D. M. Paton arrived a little later. S. Gay French, H. M. Balfour and other naval medical officers, along with Ellis, were occasional members of the group; others who sometimes took part included Haldane, D. Williams and R. G. Bickford.

Sand was elected to the Royal Society on 16 March 1944.

But then came tragedy. on 11 July 1945 at 58 West End Lane, Hampstead, Alexander Sand shot himself in the heart with a pistol. The famous coroner, Sir Bentley Purchase recorded the verdict of the inquest on the death certificate, ‘dec[ease]’d did kill himself not being of sound mind’. I have been unable to find any press reports that might shed more light on the events leading to his death. There is no mention on the death certificate of service in the navy (occupation shown as .F.R.S. and Doctor of Science’). However he is listed as having died while still serving in the RNVR. His nominal ‘ship’ (all sailors are attached to a ship, even if that ship is a shore establishment) was H.M.S. Victory, the shore establishment at Portsmouth.

Russell concluded his obituary notice:

The whole Plymouth staff were anxiously looking forward to the day when they would once more be reunited at the laboratory and the blow was bitter when it was known that Alec Sand would not be numbered among those returning. Having reached the height of his research powers it was anticipated that he would open up new avenues in the little explored field of the sensory environment of marine animals. All alike felt keenly the loss of a friendly and inspiring colleague, and a gap has been created in the ranks of physiologists that it will be hard to fill. 

Thomas Alan Stephenson (1898-1961, FRS 1951), Lancelot Hogben’s successor in Cape Town until returning to Britain in 1940 as professor of zoology at Aberyswyth, introduced his obituary of Sand in Nature as follows:

In the completely unforeseen death of Alexander Sand at the age of forty-three, comparative physiology suffered a very severe loss. Not only was his later work distinguished in a remarkable degree, but so much more of the same calibre might have been expected from him in the next twenty years. 

UPDATED 11 October 2020

*Hogben claimed he had forgotten the name of his predecessor, ‘a dedicated necrophilist’. It was John Dow Fisher Gilchrist (1866-1926), a marine biologist born in Scotland, who, in his time, seems to have been far more modern in research, but not in teaching perhaps, than Hogben indicates.

1. David Slome (1906-1995). Details here.

2. I can find no further information on Joyce Eyre.

Alexander RMcN. 2001. Otto Egon Lowenstein. 24 October 1906 - 31 January 1999: Elected F.R.S. 1955. Biographical Memoirs of Fellows of the Royal Society 47, 357-368.

Hogben, LT. 1998. Lancelot Hogben. Scientific Humanist. Woodbridge, Suffolk: Merlin Press.

MacIntosh FC, Paton WDM. 1974. George Lindor Brown 1903-1971. Biographical Memoirs of Fellows of the Royal Society 20, 41-73.

Stephenson TA. 1945. Dr Alexander Sand. Nature 156, 383-384.

Russell FS. 1948. Alexander Sand 1901-1945. Obituary Notices of Fellows of the Royal Society 5, 803-815.

Wells GP. 1978. Lancelot Thomas Hogben 9 December 1895 - 22 August 1975. Elected F.R.S. 1936. Biographical Memoirs of Fellows of the Royal Society 24, 183-221.

Zoond, A. 1933. The mechanism of projection of the chameleon’s tongue. Journal of Experimental Biology 10, 174-185. 

Zoond A, Bokenham NAH. 1935. Studies in reptilian colour response. II. The role of retinal and dermal photoreceptors in the pigmentary activity of the chameleon. Journal of Experimental Biology 12, 39-43.

Zoond A, Eyre J. 1934. Studies in reptilian colour response. I. The bionomics and physiology of the pigmentary activity of the chameleon. Philosophical Transactions of the Royal Society B. 223, 27-55.

Joan Procter. Her Reptile House at London Zoo and Reptilian Thermoregulation

It is only when one reads the detail of Joan Procter’s Reptile House at London Zoo that one realises she was decades ahead of her time in terms of knowledge of the thermal requirements of reptiles. The Reptile House opened in June 1927. Apart from its ‘aquarium-principle’ lighting, crowd circulation and safe-handling area for venomous snakes, the spectra of both natural and artificial lighting were specified while additional heat was supplied to different places of the cages thus creating a temperature gradient which allowed the animals to bask and raise their body temperature above that of their surroundings.

In Joan Procter’s own words when describing how the Komodo Dragons were housed and how they had lived in the new Reptile House for 18 months:

They live in a large enclosure of natural shingle and soil, planted with living palm-trees, and provided with a cave, rocks, and a swimming-pool. A great deal of care has been exercised to provide proper climatic conditions. The roof is of Vita-glass, transparent to ultra-violet light, and Vita-lamps for artificial sunlight are installed together with two large flood-light lamps. Dull-heat radiators of the beam type are also fixed, and all this apparatus, which is invisible to the public. is protected by massive steel bars. Further, the rocks themselves are electrically heated with a type of black-heat radiator let into the actual rock, and controlled, together with the air-heaters by a thermostat, which in turn is governed by a fool-proof warning system. The light and heat are chiefly focussed on a large rock in the centre of the enclosure, and, as the dragons immediately discovered this, they are usually to be seen sunning themselves upon it.

Those who know anything about reptiles will recognise this as a throughly modern way of keeping lizards. As I pointed out in a previous article the Vita glass was to let ultraviolet rays in sunlight reach the animals. Her ‘Vita-lamps’ were actually ultraviolet-emitting lamps with Vita glass filters to block just the very short wavelengths which experiments had determined were deleterious.

Previously, reptiles kept in temperate climates were kept in accommodation heated to the temperature of a tropical shade environment. Most had no opportunity to bask and raise their temperature above the ambient. The science of thermoregulation in reptiles really only took off in the 1940s and the concepts like ‘preferred body temperature’ and  ‘behavioural thermoregulation’ developed. Thus while reptiles are indeed cold-blooded they were found able to maintain body temperatures above that of their surroundings during the hours of daylight by shuttling between the heat of the sun and the relative cool of the shade. Komodo Dragons have been shown, comparatively recently, to follow that pattern.

The preferred body temperature was later shown to be that which is optimal for biochemical processes within the body. Reptiles not allowed to achieve their preferred body temperature, even though kept in warm ‘tropical’ daytime air temperatures, were function sub-optimally. It is not surprising that such animals are lethargic, their immune system left unable to cope with infection and infestation, do not breed—and do not survive for very long. Reptiles, particularly larger ones, take a long time to die.

Joan Procter was aware that she had designed accommodation for Komodo Dragons that was superior to that elsewhere. She quoted from William Douglas Burden’s book Dragon Lizards of Komodo (see my article on the Burden expedition to Komodo here):

     …We hear of specimens taken to New York* that “it was painful to see the broken spirited beasts that barely had strength to drag themselves from one end of their cage to the other.”     ‘’"SureIy it is not all a matter of diet and change of climate... Perhaps…Varanus komodoensis, in order to survive, demands the freedom of his rugged mountains.” ...,but our specimens are perfectly happy in captivity, are attached to their keepers and their friends, and are putting on a great deal of weight.

I think we can take that as London 2: New York 0, 1928 style.

This photograph of a small boy and a Komodo Dragon may have been
taken in the original accommodation in the Reptile House in London
Zoo in 1932. Joan Procter and the keepers always seemed keen
to demonstrate how tame the Dragons had become

The heating and lighting equipment was not ‘off the shelf’. The General Electric Company Ltd (not to be confused with the American company of the same name) had research and development labs at Wembley. The Times (15 June 1927) in describing the new house reported:

The very elaborate electrical installation devised by the Research Department of the General Electric Company to meet the special requirements forms an achievement in electrical installation which is unique, and cannot be described in detail here. It may be said, however, that the installation has approximately 20 miles of electric cable for the heating system and 12 miles for the indicators and tell-tales, and that some of the compartments have up to 200 electrical connexions. The wiring for lighting is almost equally elaborate.

Miss Procter wanted material for the walls that could be cleaned. She therefore had the theatrical scenic artist, John Bull, use car enamel that would be resistant to scrubbing. I cannot find a photograph of any of the scenes painted on the walls of the cages—perhaps a good job since I utterly loathe naturalistic painted backgrounds.

It is clear from contemporary diagrams that the Komodo Dragons were kept in the large enclosures at the southern end of the Reptile House, used, ever since I first went to the Zoo in the 1950s, to house crocodilians. Their glass roofs can be seen in Google Earth—just a short distance away from the new housing for Komodo Dragons.

This Google Earth View of the Reptile House shows the windows
above the cages where the Komodo Dragons were housed. Vita
glass was installed originally. Has it survived?
The new enclosure covered in plastic is the current housing
for Komodo Dragons

It is easy to criticise—ninety years after it opened—aspects of the Reptile House. The compartments for large snakes seem of the wrong proportions, for example. The domestic architect but President of RIBA, Guy (later Sir) Dawber (1861-1938), who took Joan Procter’s very detailed plans, made them buildable and added the external features seems to have missed a few tricks. The sides, especially the western elevation which forms one side of the alley between the equally depressing edge of the Mappin Terraces, are devoid of life. Guillery suggests the outward-facing cage on the eastern side (which often used to house interesting chelonians and is the only relief from the drabness) was inserted later. Dawber also designed—again from a detailed layout by Joan Procter and Chalmers Mitchell—the exterior of the nearby main entrance to the Zoo in the same Italianate style used by earlier architects. I sometimes wonder if Dawber took umbrage at the minor role he was accorded by the Chalmers Mitchell publicity machine; he did not attend the opening of the Reptile House.

But Joan Procter’s house was clearly a great leap forward for the Zoo. But there was still much to learn since reptiles and amphibians died in large numbers after importation. Even the best conditions will not reverse the effects of the stress of capture, storage in unsuitable accommodation and then long sea journeys at temperatures below the optimum together with under- and/or mal-nutrition. Real advances, other than air transport, in how to keep reptiles, other than the ‘easy’ species, would not come for another four or five decades.

I can't resist showing one of my photographs of these wild Komodo Dragons
taken in 2016

*These Komodo Dragons in New York seem to have been forgotten by historians. Their arrival in USA is usually given as 1934, Washington.

Guillery P. 1993. The Buildings of London Zoo. London: Royal Commission on the Historical Monuments of England.

Peaker M. 1969. Some aspects of the thermal requirements of reptiles in captivity. International Zoo Yearbook 9, 3-8. Zoological Society of London. London: Academic Press. 

Procter JB. 1928. On a living Komodo dragon Varanus komodoensis Ouwens, exhibited at the Scientific Meeting, 23 October 1928. Proceedings of the Zoological Society of London 1928, 1017–1019.

Time to kill off the term ‘brumation’ for hibernation in reptiles

Amateur herpetology circles and zoo keepers tend to obsess over using the term ‘brumation’ instead of hibernation for what reptiles and amphibians from temperate climes do in winter. In fact the internet is infested with those correcting others on what they see as an error of terminology.

"Bill" Mayhew
From here

Brumation was a word coined in 1965 by Wilbur "Bill" Waldo Mayhew (1920-2014) of the University of California at Riverside as a result of his work on hibernation in the Flat-tailed Horned Lizard, Phrynosoma mcallii (then known as P. m’calli). Mayhew was working in the heyday of research on thermoregulation and metabolism in lizards. He had arrived at the new campus of Riverside in 1954 after education (BA, MA, PhD) at Berkeley under the G.I. Bill. He had a distinguished war record as an air gunner in B17 (Flying Fortress) and B24 (Liberator) bombers in North Africa, China and Burma*.

Mayhew called his lizard an ‘obligatory’ hibernator because no matter what the outside temperature was, those kept in his laboratory ceased to eat and became torpid at the onset of winter. Other lizards—‘facultative’ hibernators could be kept active all winter by maintaining a high temperature. Mayhew recorded that metabolic rate (oxygen consumption) fell to an extent greater than that which would be expected from a fall in environmental temperature. For example, if the lizards were cooled during summer, metabolic rate fell but not to the extent seen in winter at the same body temperature. In other words, hibernation is some special physiological process that alters the normal relationship between body temperature and metabolic rate.

Phrynosoma mcallii
Photograph by Gary Nafis (CaliforniaHerps.com)

A decrease in metabolic rate independent of a decrease in temperature means of course less energy expenditure even if the temperature of the hibernaculum is high in the desert sunshine of autumn or early spring. In terms of running off body stores to maintain life during winter, a metabolic rate lower than that brought about simply by a fall in temperature would be of obvious survival value.

In the summary of his paper, Mayhew wrote:

The term brumation is proposed to indicate winter dormancy in ectothermic vertebrates that demonstrate physiological changes which are independent of body temperature.

In the paper itself he expanded that argument:

Results to date show that relatively complex physiological changes occur during or immediately preceding winter dormancy in some ectothermic vertebrates. To this extent, these animals are similar to hibernating birds and mammals. However, they differ from these heterotherms (see Cowles, 1962) in their inability to control their body temperatures. Consequently, it seems advisable to have one term to designate winter dormancy in heterotherms and another for such ectotherms. Hibernation has been used to denote this condition in heterotherms particularly, so it seems best to retain this term for that group of vertebrates. Therefore, I propose the term brumation (from bruma, L. winter) to indicate winter dormancy in ectothermic vertebrates that demonstrate physiological changes which are independent of body temperature.

Now, there are three points. Firstly, the similarity between ‘heterotherms’ and Mayhew’s ectotherms is greater than the difference. Both have mechanisms to lower metabolic rate, irrespective of the body temperature. Secondly, Mayhew’s definition limits it application to reptiles, or amphibians, or fish, in general since it applies to those ‘that demonstrate physiological changes which are independent of body temperature’. Mayhew did not know what happened in other reptiles—or amphibians—or fish. To apply ‘brumation’ to all would imply one adaptation for hibernation in all poikilotherms and that notion would need to be tested in a wide number of species. Thirdly, I have found nothing to suggest that Mayhew himself intended his term to apply to all reptiles or all poikilotherms. Therefore, if you use the word hibernation to describe winter dormancy, which makes no assumption about the physiological mechanisms involved, you will never be using the wrong term; with brumation you may well be wrong.

Others have questioned, indeed, slightly ridiculed, Mayhew’s now 50-odd year old neologism, as explained here in what seems to be a defunct blog.

This house gecko, Hemidactylus bowringii, I photographed
in Hong Kong in 1966

I was reminded of my long-standing objection to the use of brumation when I found in a pile of papers the notes for a talk I had given in May 1967 to the Hong Kong Natural History Society. I must have just read Mayhew’s paper because I asked the question not only what happened to reptiles during the winter in Hong Kong but also what happened to their metabolism. The reason I did so is because Hong Kong lies just within the tropics but does experience spells of relatively cold winter weather. Hibernation, I argued, would be short and perhaps interrupted. Indeed, when I was looking up John Romer’s early herpetological activities in Hong Kong during the late 1940s, I came across his observations:

In the colder weather [in Hong Kong] geckos either disappear altogether into hibernation or are very much less active. Here is my house there are several specimens of our very common house gecko, Hemidactylus bowringii and since their disappearance into hibernation last year I noticed two of these for the first time on the 15th February. I did not see either of them again until the 29th February [1948 was a leap year] when one of them was seen. They seemed to disappear again until the 7th March and were then seen quite frequently always in the same part of the house.

The question I asked then—and still have no answer now—is whether Hong Kong reptiles and amphibians faced with variable winters of relatively short duration behave like the North American desert lizards studied by Mayhew and others, in that they have a mechanism to lower their body rate independently of their body temperature, i.e. brumate by Mayhew’s definition, or do they simply lapse into cold torpor for a few weeks or even days, with their metabolic rate simply matching the decrease in temperature?

Golden Kukri Snake. Just off Route Twisk near the road to
the summit of Tai Mo Shan. 1968

But there is a second question. Do all Hong Kong reptiles and amphibians use the same mechanism to cope with low winter temperatures? House geckos living on, say, the tip of Kowloon near the sea could face a very different set of circumstances from the Golden Kukri Snake (Oligodon cinereus) we found in 1968 at about 500 metres altitude just off Route Twisk or the Mountain Pit Vipers (Trimeresurus monticola) found around 900 metres on Tai Mo Shan where frosts are sometimes recorded.

In summary, brumation: (i) unnecessary since it has no explanatory value (ii) can, possibly, be positively misleading when applied indiscriminately, (iii) time, therefore, for the term to join the dead parrot in the choir invisible.

My binning of brumation in no way detracts from the work that Mayhew did nor his reputation as a  physiological ecologist and academic field naturalist. He was a co-founder of the University of California’s Natural Reserve System for field studies. A dormitory for visiting scientists on the Philip L. Boyd Deep Canyon Desert Research Center is named in his honour, as is a new chair in the university.

*In his retirement he wrote Pictorial History of the 7th Bombardment Group Wing 1918-1995, published in 1998.

Mayhew WW. 1965. Hibernation in the horned lizard, Phrynosoma m'calli. Comparative Biochemistry and Physiology 16, 103-119.

A useful summary of the early work on hibernation in reptiles:
Bennett, A. F. and Dawson, W. R. (1976). Metabolism. In Biology of the Reptilia, Vol.5 (ed. C. Gans and W. R. Dawson), pp.127 -223. London, England: Academic Press.

Komodo Dragons. A peaceful morning in the Komodo National Park and an acrimonious debate on reptilian venoms

Last September’s Expedition Cruise from Darwin through the Lesser Sunda islands of East Timor and Indonesia included stops at Rinca and Komodo. Ever since my fourth cousin once removed visited Komodo in 1956 I have wanted to see Komodo Dragons alive and in their natural habitat. They did not disappoint. We saw very large males (hanging out around the kitchen of the ranger station on Rinca hoping for a hand out), females and juveniles (but not the hatchlings which apparently take to the trees to avoid their predatory parents). One female was digging out the nest mound of a megapode, the Orange-footed Scrubfowl (Megapodius reinwardt) in which to lay her own eggs, September being the egg-laying time in their breeding cycle.

When we got back I had a chance to look at and think about the various hypotheses that have been advanced as to how Komodo Dragons—and, possibly, some other monitor lizards—kill their prey. The highly publicised but never properly tested proposal that Komodo Dragons are venomous in the sense that venomous snakes are venomous, i.e. toxins delivered by injection having a very or fairly rapid systemic effect on the prey, seems to be in the process of being discarded in the course of some pretty acrimonious arguments, along with the associated hypothesis of a single, early origin of venom in reptilian evolution—the Toxicofera hypothesis. The other idea, that pathogenic bacteria harboured in the mouth of dragons causes sepsis in prey animals that are bitten but escape the initial attack, doesn’t seem that convincing or special given the likelihood of infection from a bite from any animal, as any postman will testify, especially if that postman were to immerse his bitten ankle in fetid water, as non-native water buffalo do when bitten by a Dragon. If I were to bite a Timor Deer on the leg, there is every likelihood an infected wound that could impede mobility would ensue. 

Given the opposition to the Toxicofera hypothesis and the contentious nature of the evidence for Komodo Dragons being venomous, it seems a pity that the BBC repeated last November the screening of an episode from its 2011-12 season of the Natural World Series called Komodo—Secrets of the Dragon that was devoted virtually entirely to that proposition and its main protagonist. Had this been a programme about a topic other than science-led natural history the BBC would have been falling over itself to show someone with the opposite view, however perverse. As it is, the viewing public in Britain has been left with the impression that the venomous nature of the Dragon is accepted. At the very least the BBC should have been aware of what was going on (by reading Wikipedia for example) and before rescreening it should have added an annex to the original programme. That annex could have  explained the opposing views and evidence—some of which made news media reports*—that have been accumulating since 2009. Adam Hargreaves (Oxford), Abigail Tucker (King’s, London) and John Mulley (Bangor), who produced a devastating critique** of the toxicoferan hypothesis in 2015, should have been consulted and involved. But let’s leave the BBC and its usually excellent (but sometimes spectacularly poor) natural history programmes and return to the mouth of the dragon.

None of the criticisms of the venom hypothesis imply that the composition and quantity of saliva are not of selective advantage to the despatch of prey, subsequent swallowing and digestion or protection of the oral cavity against infection. Nor, indeed, do they refute the idea or evidence that saliva may have local beneficial—to the Dragon—effects on inflicted wounds, like the application of a secreted anticoagulant, for example.

The drooling mouths of some of the male Dragons we saw were impressive. The only comparable example I could think of was my late mother-in-law’s Boxer dogs given the slightest hint of finding something edible. With no obvious sign of food or feeding activity, is Dragon saliva being used for some other purpose like scent marking?

The accumulated data that I have found suggests to me that Komodo Dragons, as originally thought, kill their prey by sheer brute force from wounds inflicted by a very large mouth with very big teeth. In one study†, 17 attacks on large prey were observed, 12 were fatal. Of the 5 that escaped with injuries to their limbs and rump, 1 was quickly attacked and killed by a second Dragon, 2 died within hours, one fled being pursued by other Dragons and one limped away without being pursued. The eventual fate of the two that possibly survived is not known.

One may though ask how, if the Komodo Dragon originally preyed upon the now extinct dwarf elephant, Stegodon, of Flores, as suggested in 1987 by Jared Diamond, those beasts (smaller than a domestic water buffalo) were killed? Would biologically-active substances in saliva have been of selective advantage?

Nowhere have I found (but I am not have looked in the right place) any discussion of the selective benefits of a slow death of the prey to the predator. A snake with a fast-acting neurotoxin can quickly track and swallow its prey without that investment in metabolically expensive venom being lost to another snake or any old predator happening to find the corpse. But let’s say a Dragon does inject toxins with a small bite and the animal runs away to die. There is no guarantee that the investment in venom would pay off. With lots of other Dragons around, the prey could be lost entirely or the original killer would get only a small share in a communal but competitive feeding session. Surely, if monitor lizards are venomous at all then why have they not evolved a more effective venom to ensure a quick kill?

The venomous dragon and other monitor lizards hypothesis has been around now for ten years. I find it sad that so little has been done at the whole animal and tissue levels to test it. I found some of the original observations and experiments‡ unconvincing. But given the captive populations of Dragons and a local abundance on Komodo and Rinca, a rigorous examination of the whole question cannot be beyond the bounds of practical realisation or funding.

*e.g. Zimmer C. 2009. Chemicals in Dragon’s Glands Stir Venom Debate. New York Times, 18 May 2009. Yong E. 2015. A Venomous Fight Among Reptile Scientists. The Atlantic, 2 November 2015

*Hargreaves AD, Tucker, AS, Mulley JF. 2015. A critique of the toxicoferan hypothesis. In, Gopalakrishnakone P (ed), Malhotra M (ed). A critique of the toxicoferan hypothesis. In Evolution of Venomous Animals and Their Toxins: Toxicology. Springer Netherlands, p 1-15. DOI: 10.1007/978-94-007-6727-0_4-1

†Bull JJ, Jessop TS, Whiteley M. 2010. Deathly drool: evolutionary and ecological basis of septic bacteria in Komodo Dragon mouths. PLoS ONE 5(6): e11097. doi:10.1371/journal.pone.0011097

‡Fry BG Wroec S, Teeuwisse W, van Osch MJP, Moreno K, Ingle J, McHenry C, Ferrara T, Clausen P, Scheib H, Winter KL, Greisman L., Roelants K, van der Weer L, Clemente CJ, Giannakis E, Hodgson WC, Luz S, Martelli P, Krishnasamy K, Kochva E, Kwok H, Scanlon D, Karas J, Citron DM, Goldstein EJC, Mcnaughtan JE, Norman JA. 2009. A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus. Proceedings of the National Academy of Sciences of the USA 106, 8969-8974 doi 10.1073 pnas.0810883106