Tuesday 21 December 2021

A dissenting review of J.Z. Young’s Life of Vertebrates from 1951. Who wrote it?

I had a surprise when I found a book review in Zoo Life, a magazine circulated to fellows of the Zoological Society of London from 1946 until 1957. The review, written for the Spring 1951 issue, was of the first edition of The Life of Vertebrates by J.Z. Young which had been greeted with universal acclaim as ‘a breath of fresh air’.  As a result of its new approach generations of students were brought up with it. As I read the review I realised that the reviewer did not like it one little bit—well perhaps just one little bit since its extensive treatment of birds was praised. All the reviewer had to say on J.Z.’s treatment of fish concerned the fishing industry!

This was the first real statement to catch my eye:

The other chapters are less satisfactory. The fact of evolution being a continuous process and that it is embryologythe evolution of the individual--that alone provides a continuous chain of evidence, while the evidence of comparative anatomy or palaeontology consists of isolated fragmentsis not mentioned.

The reader in 1951 might have been taken aback by the misuse of the word ‘evolution’ as applied to the ontogeny of an individual organism. But I will not go further into questions of phylogeny and ontogeny in this article.

Then came:

Even a single palaeontological specimen may be of extraordinary interest; our knowledge that there once existed poisonous serpents of dimensions rivalling—indeed probably exceeding—those of the anaconda or of the largest pythons of the present day rests entirely on a singe tooth dug up in Gran Chaco!

Who was the reviewer? Did he not know that the identification of the tooth of a supposed giant snake by Sir John Graham Kerr in 1927 had been shot down in flames in 1939. The ‘tooth’ was a broken off projection from a conch shell, as I have explained here. Oh dear. But the review ended with:

It is to be regretted that the author has not acquainted himself with the large amount of information now available regarding the life-history of those archaic and still surviving vertebrates Polypterus, Ceratodus, Protopterus and Lepidosiren. The facts exposed by the study of these creatures have important bearings upon the old fashioned ideas on “The Life of Vertebrates”.

And who did the descriptive studies on lungfish? Sir John Graham Kerr. So it was hardly necessary to see that the reviewer, J.G.K., was no other than the man himself: Sir John Graham Kerr.

How utterly embarrassing. I wonder what J.Z. Young did with Kerr’s review. Frame and hang it in a room thought suitable for the purpose? How much it led to misconceptions of then modern zoology in the minds of the largely amateur readers of Zoo Life is anybody’s guess.

Kerr was 82 when he wrote the review and looking back on it 70 years later, he provided a contemporary demonstration quite like no other of why J.Z.’s new textbook was so welcomed as that  ‘breath of fresh air’. It also adds weight to the comment by Edward Hindle in his biographical memoir on Kerr: ‘Graham Kerr was a man of very vigorous personality and aroused strong opposition in certain individuals’.

It was Hindle who would, as editor, have solicited the review of The Life of Vertebrates in Zoo Life. He left the Zoological Society of London where he was scientific director in the same year. Previously he had succeeded Kerr in the regius chair of zoology in Glasgow and the two were related by marriage. And it was Hindle who perpetuated the mischief of the hypothetical giant snake when writing Kerr’s biographical memoir; nor did he get to grips with Kerr’s overweening views on the value of morphological embryology in matters of phylogeny.

In all, a rather sad but historically informative snapshot. The take-home message that J.Z. put across is as relevant today as it was when he wrote it:

…every biologist must know as much as possible of the life of the whole organism with which he deals…

Sadly, 70 years on that message and the integrative approach has, to a great extent, been forgotten as biological science has been balkanised into narrow fields of research and thought.

Friday 17 December 2021

Introduced snakes on snake-free islands are bad news. The California Kingsnake on Gran Canaria devastates the local lizard populations

Did you know that an introduced snake is having a devastating effect on the three endemic lizards of Gran Canaria? No, me neither but a paper published this month spells out what has been happening.

The California Kingsnake (
Lampropeltis californiae) became one of the most popular snakes kept and bred in captivity from the 1970s. The story from Gran Canaria, where there are no native snakes, states that they were first found in the wild in 1998 after ‘the release or mass escape of individuals bred in captivity’. Since 2007 it has been found in first one, then two and then three distinct areas and various efforts have been made to control the population.

The research described in the new paper has estimated the effects of the snake’s presence by comparing areas where it is known to occur and those in which it does not (yet). There are three species of reptile on Gran Canaria, all endemic to the island. One, the Gran Canaria Giant Lizard, Gallotia stehlini, was reduced in numbers by 90% in the sites where the snake was present; the second, the Gran Canaria Skink, Chalcides sexlineatus, by 80%; the third, Boettger’s Wall Gecko, Tarentola boettgeri, by 50%.

Lizards are not the only prey. The endemic birds of the Canary Islands are also eaten as are feral mice and rats. Not surprisingly, efforts have been—and continue to be—made to eradicate the snake from the island.

This California Kingsnake I kept in the early 1970s. Kingsnakes are
famous for killing and eating other, often venomous, snakes.
I had to put this one in a vivarium holding a much heftier Royal
Python for a couple of minutes. When I returned I found the
kingsnake trying to constrict the python. Had I not intervened
would it have succeeded?

Gallotia stehlini is a magnificent lizard, reaching 80 cm in length.
I had a pair in the 1980s but passed them on to somebody with
more room. They breed readily in captivity and are omnivorous.
Photo: Juan Emilio from Las Palmas de Gran Canaria - on Wikipedia

Piquet JC, López-Darias M. 2021 Invasive snake causes massive reduction of all endemic herpetofauna on Gran Canaria. Proc. R. Soc. B 288: 20211939. https://doi.org/10.1098/rspb.2021.1939 

Sunday 12 December 2021

Scientists who kept animals. 1. Parr Tate, Canaries and Antimalarial Drugs

There are those who think people who keep or have kept animals (excluding pet dogs and cats) are strange. On the other hand there are those of us who think that those who do not keep animals are the oddities. It was while writing a Royal Society Biographical Memoir that it struck me that I should start a series on scientists who kept animals as a hobby or professional sideline, the latter activity in many cases not only stimulating an interest in the animal life but also contributing to success in the former. The trail I was following was in a field, parasitology, of which my knowledge is rudimentary. In a biographical memoir on Ann Bishop FRS (1899-1990), Len Goodwin FRS (1915-2008), the subject of the memoir I was co-authoring, and Keith Vickerman FRS (1933-2016) who when we used to meet for lunch in the late 1990s up to his serious accident in 2002 told me about some of his work on how trypanosomes avoid the host’s immune system, wrote:

In 1927…the Medical Research Council joined in the search for new antimalarial drugs. With money from the Council, compounds were synthesized in the chemistry departments of several universities and sent for testing for antimalarial activity at the Molteno Institute. At that time, the only infection available for laboratory tests was Plasmodium relictum in canaries, the vector being Culex pipiens. The uniqueness of the Molteno Institute in the testing of antimalarial drugs was due to Dr Parr Tate, an Irishman with a boyhood interest in breeding canaries and a regular prize winner at local shows in Cork.

Parr Tate (1901-1985) arrived at the Molteno Institute in Cambridge in 1924. After suffering severe asthma as a boy which meant that he could not attend school, instead relying on private tuition,  he had graduated from University College, Cork in 1923 and then completed an M.Sc. He stayed at the Molteno for 44 years, becoming its Director in 1953 until his retirement in 1968. Thereafter he divided his time between Cambridge and Cork with his sister; he died there in 1985.

Tate’s interest and skill in keeping, breeding and exhibiting canaries may not just have contributed to his later scientific career. Canaries and other birds are now well known to be responsible for some cases of asthma (Bird Fancier’s Asthma) in their keepers and others in the household.

Crompton DWT. Parr Tate, 1901-1985. 1986. Parasitology 93, 249-250. https://doi.org/10.1017/S0031182000051416

Goodwin LG, Vickerman K. 1992. Ann Bishop 19 December 1899-7 May 1990. Biographical Memoirs of Fellows of the Royal Society, 38: 28–39.  doi:10.1098/rsbm.1992.0002

Thursday 9 December 2021

Monkeys and Vitamin D. Pioneering science successfully applied to wild animal husbandry in the 1920s and 30s by Miss Hume, Miss Smith and Dr Lucas

The story of the discovery of Vitamin D in the early decades of the 20th century as part of an effort to cure rickets is well known to historians of endocrinology and nutrition. What I did not know until I looked in some editions of Zoo Life magazine was the rôle that monkeys kept as pets, at London Zoo and at the Lister Institute played in the early days of the story.

The article written in 1951 by Margaret Hume and Hannah Henderson Smith under the title ‘Monkeys and Sunshine’ began:

Twenty-five years ago monkeys in captivity used to suffer from cage paralysis. They lost the use of their limbs, sat about listlessly and gradually faded away. We know now that the disease was really the same as human rickets and that what the monkeys lacked was sunshine.

Eleanor Muriel Margaret Hume (1887-1968) and Hannah Henderson Smith (1885-1972) were nutritionists working at the Lister Institute in London. Hannah Henderson Smith served in Queen Alexandra’s Imperial Military Nursing Service during the 1914-18 War; she became Acting Matron of the military hospital at Fovant in Wiltshire. After the end of the First World War they were sent as half of a team led by Hariette (later Dame Hariette) Chick (1875-1977) to Vienna to investigate nutritional diseases which were then rife in the city. They established in their two-year stay at the children’s hospital that cod liver oil or exposure to ultraviolet light could cure and prevent rickets in children.

The article continued: 

Having seen miracles of healing and of relief from pain achieved in Vienna with the aid of light and cod-liver oil, and being monkey lovers, convinced that monkeys in confinement in Britain were the sun-starved victims of the colder climate which kept them indoors, we decided on our return to England to test our belief.

There was no lack of subjects for experiment. Many people, from publican to peer, were monkey lovers too. They heard about our work from the pet shops and brought their bent and crippled pets to us at the Lister Institute for treatment with ultra-violet light. There was no doubt about its success. The crippled creatures began to walk again, even though on deformed limbs. In spite of difficulty we had X-ray photographs taken of a few and were able to demonstrate the restoration of bone which was the basis of the cure. Our experience in curing these invalids and our success in advising their owners how to keep them in health made it clear to us that, once the supply of vitamin D was in some way assured, the major obstacle to keeping many of these creatures healthy in captivity was removed.

They acquired monkeys for themselves to see if they could get them to breed. The first they chose were a pair of Common Marmosets (Callithrix jacchus but then known as Hapale jacchus). They were commonly available in British pet shops, particularly in London, and had a short lifespan in captivity. Each day the marmosets were exposed to ultraviolet radiation from a mercury-vapour lamp. Not only did that pair breed, the first successful breeding of this species in Britain, but another pair produced 25 young over the years and a number of grandchildren. They then went on to see if they could keep Squirrel Monkeys (Saimiri sciureus, then S. sciurea) since London Zoo failed to keep them successfully. Initially so did Hume and Smith but after one of their’s died, an autopsy revealed rosary of the ribs, a characteristic of rickets. Therefore they upped the length of daily exposure to ultraviolet for the next Squirrel Monkeys they obtained. That pair lived together at the Lister Institute for ten years, every day being exposed to ultraviolet for half an hour. They thrived but did not breed. Then their lab was evacuated to Cambridge (to occupy the house of the Lister’s Director) and the monkeys had to live in a glazed conservatory (glass blocks ultraviolet radiation from the sun) with no means of running the mercury-vapour lamp. The monkeys began to deteriorate and the male died within a couple of months. I have told the story of ‘Vitaglass’ and its pioneering use at London Zoo previously; it did not block the sun’s ultraviolet rays. Two panes were obtained and installed instead of glass in the conservatory. The remaining monkey’s cage was moved close to the panes of Vitaglass. She responded to the winter sun shining directly into her cage: ‘She curled up in it, making a happy noise like sleigh bells with which she ever afterwards welcomed the coming of the sun’.

Photograph from Zoo Life showing 'Olive' on the
shoulder of 'her best friend'. I suspect this is Hannah
Henderson Smith

In 1946, lab and monkey moved back to London but there was no mercury-vapour lamp or Vitaglass. She was therefore given milk containing Vitamin D (the form is not stated, see below). In 1949 at the age of 21 the female Squirrel Monkey (called ‘Olive’) died of old age. Olive had been entertained by the comings and goings of a busy lab; in turn she, and the marmosets, had informed her fellow primates something of the of the habits of New World Monkeys and of the necessity of Vitamin D.

The authors concluded:

In summing up the whole story, one must say that the application to the care of all these monkeys, of scientific knowledge about the supply to them of vitamin D, made it possible to study the domestic habits and life history of the marmosets, and to maintain the squirrel monkey for so long that she developed, in an intimate relationship, a psychology of interest and charm and exhibited an intelligence quite unexpected in these little monkeys.

The link to London Zoo and its experiences and evidence on keeping monkeys was provided by Nathaniel Sampson Lucas (1884-1968). He had qualified in medicine with an Oxford M.B. and was on the Medical Register from 1912. He served in the Royal Army Medical Corps in 1917-19 and then joined London Zoo as pathologist. Chalmers Mitchell in his history of the Zoological Society of London noted that he retired in 1924 (at the age of 40!) but he actually joined the Lister Institute as a voluntary worker. He worked on all sorts of things, from vitamins to trying to isolate oxytocin from the pituitary. His work often involved light, from analytical spectroscopy to the effect of different wavelengths on biological processes. Having examined many dead monkeys at the Zoo and been involved in efforts to prevent vitamin deficiencies he  noted that cod liver oil had been tried but that marmosets found it distasteful and usually rejected it.

The team of Hume, Smith and Lucas was an ideal one to tackle the problem and as the authors of the article in Zoo Life stated, the results of their work were reported in Proceedings of the Zoological Society of London in 1927 and then in 1937 as a ten-year follow-up. There were also papers in Veterinary Journal.

But that was far from the end of the story because what Hume and Smith set off was a continuing interest in Vitamin D and bone metabolism in New World monkeys in particular against a background of a spectacular increase in knowledge of Vitamin D in the following decades of the 20th century and against a continuing debate on the provision of Vitamin D and its physiological rôle in human health and wellbeing. There  have been many bumps in the road to the present state of knowledge. There were, for example, claims that depriving monkeys of Vitamin D had no effect on their bones, without the realisation dawning that animals store the fat-soluble Vitamin D in body fat and signs of deficiency only become evident when the stores are exhausted. 

The biologically active form of Vitamin D acts as a steroid hormone and has effects on a number of tissues and organs. For the purpose of the present discussion I will restrict its function as stimulating the absorption of calcium and phosphorus from the intestine. The chemical precursor of the active form, which is produced by the kidneys, is synthesised in the skin by the action of ultraviolet rays. However, precursors of the biologically active form of Vitamin D are also present in some foods that some animals eat. Plants and fungi produce one form of precursor, ergocalciferol (Vitamin D2), while animals produce and store cholecalciferol (Vitamin D3). In the absence of natural sunlight or ultraviolet rays from an artificial source, an animal becomes entirely dependent on Vitamin D provided in the food. Because Vitamin D given in large amounts is toxic, there has been endless argument on how much should be in the diet of the human population as well as of animals in captivity.

Factors also known to be important in rickets and its adult equivalent are the calcium:phosphorus ratio of the diet and the provision of Vitamin B12. The use of ultraviolet sources fell out of favour when Vitamin D additives became available for fear of damage to the eyes. However, while Old World monkeys responded to the provision of vitamins and the correct Ca:P ratio, there remained a problem with New World Monkeys, both adults and young. First, the seemed to require D3 rather than D2. Even with daily intakes of D3 sufficient for Old World Monkeys serious problems remained. Further research showed that they need Vitamin D3 in far greater quantities. Marmosets and tamarins—the ones that responded to ultraviolet rays in the hands of Hume and Smith—need a specially formulated complete food that if eaten by other mammals would cause Vitamin D toxicity. Even then, animals not kept with access to sunlight run into problems, especially the young since primate milk has low concentrations of Vitamin D even when the mother has an ample sufficiency.

Clearly, just using a mercury-vapour quartz-walled lamp, Hume and Smith did provide sufficient Vitamin D for their marmosets to thrive and breed for several generations. Modern lamps which produce a targeted spectrum are said to be in use for South American monkeys not exposed to sunlight.

The reason why—in the mechanistic sense— most but not all Old World Monkeys need more Vitamin D3, from synthesis in the skin and/or the diet has been studied since the 1980s but are beyond the scope of this article. The reason why—in the evolutionary sense—has not been, to my knowledge, yet considered. 

The need for sunlight or dietary sources of Vitamin D3 of marmosets and tamarins reminded me of our only visit to Jersey Zoo in the mid-1990s (there is still discussion about who forgot the camera). A large troupe of Golden Lion Tamarins was being kept outside and many were congregated on an earth bank. There many of them were clearly sun-bathing, exposing as large a surface area as possible to the sun. On a similar note we saw Guianan Red Howler Monkeys (Alouatta macconnelli) just sitting on the top of the forest canopy in the full sun. The Harpy Eagles that live nearby must sometimes strike lucky. I therefore end with a question: Do New World monkeys get sufficient exposure to sunlight as part of their daily activity or do they need to spend time out of the forest canopy exposing themselves to the sun, and is there a trade-off in a greater exposure to predation?

Margaret Hume
from obituary in British Journal of Nutrition

The article in Zoo Life magazine:

Hume EM, Smith HH. 1951. Monkeys and sunshine. Zoo Life 6 (1, Spring 1951), 3-5.

The original publications:

Hume EM, Smith HH. 1927. The value of ultra-violet rays in the prophylaxis and cure of rickets in

monkeys. Veterinary Journal 83, 368-372.

Hume EM, Lucas NS, Smith HH. 1929. Further Notes on the Prevention and Cure of Rickets in Monkeys. Veterinary Journal 85, 490-492.

Lucas NS, Hume EM, Smith HH. 1927. On the breeding of the Common Marmoset (Hapale jacchus Linn.) in captivity when irradiated with ultra-violet rays. Proceedings of the Zoological Society of London 97, 447-451.

Lucas NS, Hume EM, Smith HH. 1937. On the breeding of the Common Marmoset (Hapale jacchus Linn.) in captivity when irradiated with ultra-violet rays. - Il. A ten years' family history. Proceedings of the Zoological Society of London A107, 205-210.

Other publications:

Copping AM. 1970. Eleanor Margaret Hume (27 May 1887-1 April 1968). British Journal of Nutrition 24, I. 

Power ML, Oftedal OT, Tardif SD, Allen ME. 1995. Vitamin D and primates: recurring problems on a familiar theme. In Proceedings of the First Conference on Zoo and Wildlife Nutrition, AZA Nutrition Advisory Group, Scarborough, OT.

Friday 3 December 2021

What attracts a tropical frog to deposit its transported tadpoles in a particular pond? Echos of Maxwell Savage’s big idea

Earlier this year I wrote a series of six articles on this website (see below for links) on Ronald Maxwell Savage (1900-1985), a professional scientist and amateur herpetologist who made extensive studies on the breeding of Common Frogs (Rana temporaria) in the wild. Savage’s big idea was that Common Frogs are attracted to ponds for breeding by the odour emitted by algae in the water. This phenomenon, he argued, would explain the timing in response to earlier rainfall, the preference for one pond over another, why frogs do not spawn in every pond and why frogs may spawn in a pond one year but not the next.

One cannot of course extrapolate the triggers for reproduction from one species to another or, for that matter, claim that only one trigger from the environment is necessary even with one species. However, an interesting new paper on research done in French Guiana suggests that another species of amphibian uses the odour of a compound or compounds in water during a key event in its reproductive life.

The species is Allobates femoralis, the Brilliant-Thighed Poison Frog. Clutches of approximately 20 eggs are laid in the leaf litter. After 15-20 days of development the eggs hatch and the tadpoles are carried on the back of (usually) the father in batches of 1-25 to small pools where they continue their development until metamorphosis; the tadpoles are known to be omnivorous but not predatory. Frogs are known to travel hundreds of metres to deposit their tadpoles and to spread the brood between several ponds. Deposition readily occurs in artificial pools.

Choosing the right site to breed or deposit partially developed tadpoles must have been subject to pretty strong selection. Get it wrong, a pond full of predators or likely to dry out, and the result of disastrous. But what cues do these frogs use to optimise the odds of the tadpoles’ survival? Several years earlier the same group found that tadpole-transporting frogs seemed to be attracted to distant ponds containing large numbers of tadpoles of the same species. There seemed to be two possible explanations: the odour of the conspecific tadpoles was the attractant or the odour of the water or something in the water was responsible. The new paper set out to determine which.

In field experiments three sorts artificial pool (plastic plant pot saucers) were placed on the leaf litter and filled with well water. One had nothing else added. The second had tadpoles of the same species in the water. The third had poured around it ‘stagnant’ water made by steeping leaf litter in water for two weeks. All three types of pond had fresh leaf litter placed around them so as to be visually indistinguishable. In all, 60 artificial ponds were prepared.

The results were clear. Stagnant water was an attractant: 

Frogs showed a clear differential pool usage: 11 out of 15 occupied pools were pools from the stagnant water condition. Out of the 253 tadpoles deposited, 212 tadpoles were found in the stagnant water condition, 23 in the tadpole water condition and 18 in the control condition. Of the 18 adult frogs observed at the pools (four of which were transporting tadpoles), 15 were at the stagnant water condition. Sixteen frogs captured visiting pools with stagnant water condition had their closest known territory points between 3 and 50 m (median=12 m) from the pools where they were found. 

The questions now remaining are: Why do these frogs prefer depositing their tadpoles in the presence of rotting vegetation and what odoriferous constituent(s) of the stagnant water is attracting the frogs?

The authors suggest that ‘stagnant’ water may be an indicator of a pond’s permanence; one that has had time to remain full and therefore not just a temporary rain-filled depression. I do, however, have another suggestion. Could it be that the smell of rotting vegetation is indicative of a nutrient-rich environment ideal for growth of the tadpoles? The leaf-litter steeped water would be expected to contain all manner of algae, protozoa and small aquatic invertebrates—bottom of the food-chain stuff—ideal as tadpole food. A similar mix soon leads to the production of ‘infusoria’ from vegetation and air-born spores that aquarists use to feed their young fish. Identification of the chemical(s) involved will prove interesting: the odour of products of decay or of organisms using the products of decay to multiply? Could it be the case that algae are involved, just as envisaged for the Common Frog by Maxwell Savage?

Serrano-Rojas SJ, Pašukonis A. 2021. Tadpole-transporting frogs use stagnant water odor to find pools in the rainforest. Journal of Experimental Biology 224, jeb243122. doi:10.1242/jeb.243122 

The earlier articles on Maxwell Savage can be found here, here, here, here, here, here.

Wednesday 1 December 2021

Masai Mara Safari - 30 years ago: The wildebeest that do not make it

A few more photographs from the Masai Mara in September 1991. The wildebeest were moving across Masai Mara and crossing rivers. Many had been drowned the night before. The Marabou Storks and vultures were gorging themselves while the smell of the corpses from earlier drownings was interesting. Breathing through the mouth with the tongue tucked down helps by the way.