Doflein’s Salamander

Some salamanders are very strange beasts. None more so than the tropical Central American species in the genus Bolitoglossa. They can shoot their tongues to catch prey like a chameleon, they can shed their tail when threatened just like many lizards, and they breed entirely on land. They belong to the group of salamanders—the Plethodontidae—that have no lungs, relying on gaseous exchange through the skin. The bolitoglossines are sometimes called climbing salamanders because they can and do live in trees and shrubs, a fact difficult to accept when seeing one for the first time since they not only have webbed feet but appear stiff and ungainly. But the fleshy, webbed feet are deceptive. When planted on a leaf and arched they act as suction cups.

I was barely aware of the existence of these salamanders in the years I first became interested in reptiles and amphibians. They do not get a mention in the popular books available in the 1950s and 60s in Britain that were written by Doris M Cochran or Robert Mertens.

About 30 years ago, I was given a few to keep by whom I cannot remember and my records have disappeared. Individuals of one species were beginning to appear on animal dealers’ lists. That species was Bolitoglossa dofleini from Guatemala, Honduras and Belize. At the time there was no commonly used name. Now IUCN list the following: Alta Verapaz Salamander, Doflein's Mushroomtongue Salamander, Doflein's Salamander, Palm Salamander. It was first described and named by Franz Werner (1867-1939) after Franz Theodor Doflein (1873-1924) who collected the salamander on an expedition to Central America in 1898.

Doflein's Salamander
One of the ones I tried to keep 30 years ago

     

Only years later did I learn that my experience of trying to keep this species was the same as everybody else’s. They appeared to live and feed perfectly well but after a few weeks or months they became lethargic, shed their tails and died. I was annoyed and puzzled that I was unable to keep animals that initially had appeared fit and healthy. Had I got something wrong or did they have some disease that developed with time?

In 2004 a note appeared in Veterinary Record. The authors made the general observation that B. dofleini ‘is generally considered notoriously difficult to keep alive; most imported animals do not survive beyond the first two months after importation’. Three males and two females, recently imported into Belgium, became anorexic and apathetic over a one- to two-week period. Then the hands and feet appeared slightly swollen and began to point upwards. Finally, the tail was shed and the salamanders died 2 to 10 days later.

At this time there was growing realisation that the chytrid fungus, Batrachochytrium dendrobatidis, was having devastating effects on amphibian species throughout the world. The authors of the paper found large numbers of chytrid cells in the cornified layer of the skin all over the body. The origin of the infection could not be determined because the salamanders could have been in contact with other animals in transit to Europe or in the dealer’s premises from which they were obtained.

The suggestion the authors made was that proliferation of the chytrid in the skin might have compromised gaseous exchange in these lungless amphibians. Kidney damage in the form of hyaline droplets was also present but whether this was related to the presence of chytrid was not known. A strange finding in three of the animals was the impaction of the stomach with moss and wooden particles.

I remained puzzled after reading the report in Veterinary Record. While clearly demonstrating the presence of chytridiomycosis, I really could not decide if the animals had died OF or WITH the disease.

Around 1990 the only information I could find indicated that Doflein’s Salamander was found in lowland rainforest. I therefore kept them at temperatures appropriate to that low altitude in Central America. However, I began to wonder if the temperature was too high. Later publications showed an altitude range of 50-1500 metres in the wild including premontane to lower montane wet forest. I did not know where the ones I was given had been collected but if they were from, say, an altitude of 1000 metres, I should have tried keeping them 10°C below that of my simulated lowland tropical environment. I have found suggestions in online fora that people attempting to keep and breed these fascinating amphibians had also tried too high a temperature. In this respect, I read there has been controversy in the past over the altitudinal distribution of the largest of the bolitoglossine salamanders, e.g. B. dofleini, that rely on oxygen uptake through the skin. One view was that large lungless salamanders can only occur at relatively high altitude because the oxygen requirements of the tissues at the higher temperatures of lower altitudes cannot be supplied by the relatively small surface area of the skin. Others have contested that view. However, cutaneous oxygen uptake compromised by the presence of chytrid together with a high environmental temperature in captivity might just have created the perfect patho-physiological storm. 

I discovered that from their size the salamanders given to me must all have been females; males are much smaller. Collectors apparently searched the leaf litter and because the females tend to live there while the males prefer to clamber in the trees and bushes it was mostly females that were imported into Europe.

The only success at keeping B. dofleini I have come across is at Fort Worth Zoo. It was reported in 2012 that ten (all females) had been kept for 6 years. On arrival, all had been treated for chytridiomycosis. I have not seen any reference to the environmental temperature in their exhibit. I have been unable to find in the various papers, whether or not those exported for research have been kept successfully for any length of time.

Fortunately, no licences are now issued for the collection of any species of Bolitoglossa (which occur in Central and the north of South America). B. dofleini takes 10-12 years to reach sexual maturity. Thus a breeding population could, by uncontrolled collection of adults, be reduced to dangerously low levels very quickly. IUCN classify the species as Near Threatened.

It does, though, concern me that nobody has a method for breeding any species of Bolitoglossa in captivity—or at least if they have, nothing seems to have been published. The radiation in these salamanders has been so great that they represent 40% of all the tailed amphibians of the world. If—perish the thought—a captive-breeding programme became necessary to ‘lifeboat’ a conservationally important species, there would be very little background knowledge with which to start.

The only consolation of my experience with Herr Doflein’s Salamander was that I did get to see but not to record the remarkable tongue in action. It can be projected up to 31% of body-length in that species in under 20 milliseconds. The maximum velocity achieved was 7 metres per second and  the maximum acceleration 4500 metres per second per second. In other words the sticky tongue hits the prey at a speed of 25 km per hour, less than 0.02 seconds after launch. The performance of the paired tongue projector muscles ‘exceeds the greatest maximum instantaneous power output of vertebrate muscle by more than an order of magnitude’. 

Here is the video made by Stephen Deban, one of the authors of the paper on the high-power tongue projection in another species of Bolitoglossa, B. franklini:

Deban SM, O’Reilly JC, Dicke U, van Leeuwen JL. 2007. Extremely high-power tongue projection in plethodontid salamanders. Journal of Experimental Biology 210, 655-667. doi:10.1242/jeb.02664 

Feder ME, Papenfuss TJ, Wake DB. 1982. Body size and elevation in neotropical salamanders. Copeia 1982, 186-188.

Pasmans F, Zwart P, Hyatt AD. 2004. Chytridiomycosis in the CentraI American bolitoglossine salamander (Bolitoglossus [sic] dofleini). Veterinary Record 153, 153.

Scales JA, O’Donnell MK, Deban SM. 2017. Thermal sensitivity of motor control of muscle-powered versus elastically powered tongue projection in salamanders. Journal of Experimental Biology 220, 938-951. doi:10.1242/jeb.145896 

Wake DB, Dresner IG. 1967. Functional morphology and evolution of tail autotomy in salamanders, Journal of Morphology 122, 265-306.

The Bear Pits of Bern in 1955. How not to keep bears

The coat-of-arms of Bern

The current issue of Keeper Contact deals with bears in zoos with particular emphasis on the changes in housing and husbandry over recent decades that have made it possible to keep and breed bears successfully without the inmates suffering the psychological consequences of boredom in captivity. Also included is a history of the famous bears and the bear pits of Bern in Switzerland—the epitome of old-school bear husbandry. Bern, apparently, still has its Brown Bears but housed close to—and incorporating—the modified pits in a modern artificial habitat.

As I read the article I remembered that I had taken photographs of the bear pits during a school trip to Switzerland in August 1955…and here they are, a reminder of how poorly bears were kept in the 19th and 20th centuries, this iteration of the pits having been constructed in 1857:

The bear pits shown in a painting from 1880

    

...and we did see other things in Bern on this very  brief visit but this is all I remember:

The Unintentional Free-Range Homing Hamster

The first and only Golden Hamster I kept was installed in a cage in a converted greenhouse. The cage, made by my father nearly 60 years ago, had a slanting front and could either have a glass slide for reptiles or a wire cage front for mammals or small birds. The type of cage front was of a particular type designed for housing budgerigars. The wire door swung outwards from side hinges and was fastened by an omega loop which fitted between the wires on the opposite side. One morning I went to feed the hamster or change its drinking water and noticed the door was not fastened. It was shut but not fastened as would happen by gravity with the front slanting inwards. I thought it odd and thought my father had perhaps fed the hamster and forgotten to close the door properly. About a week later he was feeding the hamster and noticed the door was not fastened, thinking I had not done the job properly.

A few days later I stepped off the central walkway onto the bare earth on the opposite side to the hamster’s cage. My foot disappeared into a hole. I excavated and found a tunnel about 10 cm bellow the surface going right round the bare earth with several interconnecting tunnels. I then realised that the hamster must have been leaving its cage at night, excavating the tunnels and then going back to the cage to eat, drink and sleep. The cage incidentally was about 120 cm from the ground. When the hamster managed to push open its door, overcoming the resistance of the omega loop, and set forth on its excursions, the door must have swung shut. The wanderer must have managed to pull back the door in some way in order to return to the cage and its sleeping place.

There are many reports of escaped animals trying to return to their cages but this was not so much an escape but an extension of the hamster’s home range. 

Domestic variety of Golden Hamster
Photo by Antony Colton on Flickr

American terrapins (or turtles): problems as pets and pests

Red-eared Slider - photograph by Greg Hume (used on Wikipedia)

Those of us who came into the biological sciences through a particular interest in reptiles and amphibians (and there are a good number of us) were sufficiently naive to believe that the few young American terrapins (turtles in US-speak) that occasionally appeared in provincial British pet or aquarist shops in the 1950s and early 1960s represented a relatively small number taken from the vastness of the U.S.A. wilds and that they were easy to keep. We were soon disabused of the latter. The unfortunate terrapins soon developed soft shells and swollen eyelids and only lasted a few months.

The problem was exacerbated was the pet trade itself. There appeared on the British market in 1959 the ‘turtle bowl’ designed it was said to house small terrapins. It came complete with a plastic palm tree and some food in the form of ant pupae. Swift passage to death was assured.

Some people were trying to get the word out that in terms of housing young terrapins had to be kept more like tropical fish. For example, Mrs Monica Green (1925-2014) who was Secretary of the British Herpetological Society for 57 years took the reviser and publisher of a second edition of a booklet published in the 1930s to task in the magazine Water Life (Volume 9, No 3)  in 1954 for repeating duff information on how to rear young terrapins. But the message was slow to get out and failed to appear in any of the British books on reptile keeping. Many pet shop/fishkeeping owners were in complete ignorance until magazines began to carry articles and information passed by way of mouth on just what equipment and food were needed to keep these animals successfully.

I must know make a sideways leap because we often forget most scientists setting out to be just that went—and perhaps still go—to university without ever having seen a scientific paper. Having to wade through long and tortuous papers and reviews for evenings on end came something of a shock. I supposed I was more fortunate than most because I had joined, at the suggestion of George Boyce, the British Herpetological Society in 1961. The subscription was modest and its journal was posted to members. It has to be said that the papers in the journal at that time were of highly variable quality but the problem in those days was to get sufficient papers to publish not on what percentage had to be rejected. But one which I think, with hindsight, influenced me greatly was entitled, ‘The care of young red-eared terrapins (Pseudemys scripta elegans) in the laboratory’. There were proper scientists describing how they had developed a protocol for keeping terrapins in terms of such factors as temperature, light, ultraviolet radiation/vitamin D, food and calcium supplementation. It showed me that a bit of science and a bit of empiricism could make it possible to keep animals successfully. The authors were Brian Blundell Boycott and M.W. Robins.

Brian Boycott FRS
from Biographical Memoirs
(see below)

Brian Boycott (1924-2000, elected FRS 1971) was a neuroscientist. He got a first degree in zoology the hard way—the very hard way—by part-time student at Birkbeck College, London while working to support himself. His first job was as an animal attendant at the National Institute of Medical Research, then in Hampstead, so he was ideally placed later to have both the experience and knowledge to find out how to keep animals in optimal conditions. His biographer, Heinz Wässle, wrote:

He learnt animal care the hard way and, more importantly, he was exposed to people with no academic ambition or background, to people who had sets of values and motivations different from those he had experienced. In retrospect this experience left its traces on his character. Brian socialized easily with people from greatly different backgrounds. Forty years later, at the Max Planck Institute in Tübingen, he became a good friend of Herr Baur, one of the people who worked in the animal house. Herr Baur owned a small farm with a vineyard and produced his own bread, delicious sausages, excel- lent wine and apricot brandy. Every so often Brian pretended that he was not hungry when the members of the laboratory went for lunch. Instead he secretly enjoyed a frugal lunch with Herr Baur in the animal house…

There must have been a realisation that with the ready supply from the USA young terrapins could be ideal candidates for some research. Boycott and Guillery used them to study memory. Similar advice on the care of terrapins in in the laboratory world to that formulated by Boycott and Robins was being promulgated in the U.S.A. and in Britain by the late 1950s.

Later, in the 1960s, Dr Edward Elkan (1895-1983), the father of reptilian pathology, investigated the  ‘eye disease’ of small captive terrapins. He found that the effects were widespread throughout the body and due to the lack of Vitamin A in the diet.

Edward Elkan
(from here)

Eventually, after what Elkan described as an ‘annual holocaust’ of imported animals, the word spread amongst amateur herpetologists and then to pet owners and pet shop owners. Terrapins could be reared to adulthood.

But then another problem was recognised. The majority of hatchling terrapins were hatched on ‘turtle farms’ in the southern states of the USA where they and the adults were fed on the waste from chicken processing factories. Salmonella was rife in chickens and so infection was passed to the terrapins and thence to the mouths of children and adults handling the animals or touching the water in which they were housed. While each outbreak of Salmonella from terrapins affected the market for a time, the trade remained vast especially during the Mutant Ninja Turtle craze.

No good turn goes unpunished for now pet owners throughout the world had the knowledge and the products to rear terrapins to adulthood. But there is a lot of difference between the cuteness of a baby terrapin and that of an adult the size of a plate. They may bite; they eat a lot of food and the water soon becomes foul. Many people in Northern Europe found they could no longer house their pets and zoos were inundated with cast-offs. Then, because there was no way to get rid of unwanted pets, they were released into ponds, reservoirs, rivers and streams. Fortunately, in Britain, for example, the temperatures are too low for successful hatching of eggs in the wild and like most of Northern Europe have escaped the long-term consequences of their release even though they live for decades. By contrast, in warm places like Hong Kong, Red-eared Terrapins have become an important invasive species. Not only is there a very large urban population keeping pets and releasing them when they outgrow their tank, but Buddhists have released them in large numbers in order it is said to bring good karma. There are now Red-eared Terrapins (now renamed Trachemys scripta elegans) over the place: reservoirs, fish ponds and large populations in the parks on Hong Kong island. The local relatively common species has declined.

A number of countries have acted to limit the movement of young terrapins from and within the USA, starting on public health grounds after the Salmonella scares but now because of the potential and demonstrated damage to native fauna. For example, the EU for example banned the import, sale or transfer of ownership of Trachemys scripta in 2016. But the trade in Hong Kong, Singapore and much of the rest of the world where imported terrapins have already or have the potential to cause damage continues.

Over a period of thirty years, a solved animal welfare problem morphed into an unforeseen conservation blight.

Boycott BB, Guillery RW. 1962. Olfactory and visual learning in the Red-eared Terrapin, Pseudemys scripta elegans. Journal of Experimental Biology 39, 567-577.

Boycott BB, Robins MW. 1961. The care of young red-eared terrapins (Pseudemys scripta elegans) in the laboratory. British Journal of Herpetology 2, 206-210.

Elkan E, Zwart P. 1967. The ocular disease of young terrapins caused by vitamin A deficiency. Pathologia veterinaria 4, 201-222.

Wässle H. 2002. Brian Blundell Boycott. 10 December 1924-22 April 2000. Biographical Memoirs of Fellows of the Royal Society 48, 51-68.

The Rhinoceros That Died in Nottinghamshire in 1754

Each issue of Archives of Natural History produced by the Society for the History of Natural History usually contains much that is interesting and informative. The current issue is no exception. As I was leafing through it, my eye fell on the account a rhinoceros in Nottingham in the 1700s.  A rhinoceros in Nottingham—and Derby—and even Edinburgh—in the 1700s? I was soon reading the whole article.

By searching in digitised newspaper archives Caroline Grigson of the Institute of Archaeology at University College London has added to what was already known of the import and display of Indian rhinoceroses in Britain in the 18th Century¹. The first, a female, arrived from Calcutta on 1 October 1737 (a male had died en route); the second, a male, in 1739; the third, a female, probably in 1756.

There is a long tradition of curiosities being taken around the country to be exhibited at fairs and at inns and public houses by showmen, either as individual animals or in the larger menageries seen at fairs, wakes and circuses. But the toting of an adult rhinoceros around Britain must have presented a considerable logistical challenge. Grigson, shows that the first animal was in London in 1740 and 1741 when she was “upwards of five foot high” and “twelve feet two inches from the nose to the rump”, Derby in 1742 (112 miles from London) then Burton-on-Trent and Lichfield before returning to Derby. She is recorded in Norwich in 1744 and then in 1747 in Edinburgh (over 400 miles from London). In 1749 she was back in England, at Nottingham. By the end of 1751 the female rhino was in London, housed in several inns in succession (one presumes in the stables); at this time she weighed 80 cwt or, whatever the definition of hundredweight being used, 4 tonnes or so. Somebody else can do the calculation of how many horses were needed to pull such a load along the turnpikes.

The paragraph which caught my eye initially was on the demise of the rhinoceros:

     The noble rhinoceros took to the road again and died shortly before 8 March 1754 when it was reported in the Derby Mercury that

The famous rhinoceros which was about four Years ago shewn in the White-Hart in this Town…was taken ill upon the Road from Mansfield to Nottingham, and died upon the Forest, near Red-Hill, on Thursday, to the great Loss of the Proprietor, Mr Pinchbeck. Who purchased it of Mrs Parsons some time since…

Redhill is four miles north of Nottingham on the road (now the A60) to Mansfield. In the 1700s and beyond a guide could be hired to ensure that the traveller did not get lost in Sherwood Forest, the southern limit of which was Redhill.

So, there is a conversation stopper for the pubs of Nottingham tonight. If you are tired of the endless discussion of the performance of County and Forest on the football field or the less than perfect start to the cricket season for the county side at Trent Bridge, just ask the question: Did you know an Indian rhino died at Redhill in 1754? You could also muse on what happened to the beast after it died and whether its skin and skeleton were preserved somewhere in the hope of making a profit after its loss as a live exhibit to the proprietor. Finally, as your friends’ eyes glaze over you could point out that the first rhino to reach Nottingham was not the first rhino to reach London. That one arrived in 1684 on the East Indiaman Herbert under a Captain Udall².

A very much alive Indian Rhinoceros
Kaziranga National Park, Assam, 2007

¹Grigson C. 2015. New information on Indian rhinoceroses (Rhinoceros unicornis) in Britain in the mid-eighteenth century. Archives of Natural History 42, 76-84.

²Rookmaaker LC, Jones ML, Klös H-G, Reynolds RJ. 1998. The Rhinoceros in Captivity. A list of 2439 Rhinoceroses Kept from Roman Times to 1994. The Hague: Kluger.