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 embryology—the evolution of the individual--that alone provides a continuous chain of evidence, while the evidence of comparative anatomy or palaeontology consists of isolated fragments—is 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.

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 

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

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.

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.


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.

Bruce S Grant’s book ‘Observing Evolution’ and observing scientists who wrote on evolution

I have enjoyed reading Bruce Grant’s book Observing Evolution (Johns Hopkins, Baltimore, 2021) which describes his work from the early 1980s on industrial melanism in the Peppered Moth. Grant illustrates just how difficult it is to devise experiments on a natural phenomenon and how many traps for the unwary lie in the way. However, the reason for writing this article is not to go over old ground on the status of industrial melanism since despite the efforts of an American science writer to disparage the work of Henry Bernard Davis Kettlewell (1907-1979) in Oxford, the concept we first heard about at school is, thanks to the extensive work of the late Michael Majerus (1954-2009) and Bruce Grant himself, among others, even more firmly established than it was in Kettlewell’s time. Nor is to discus further one of the key rules of life: avoid reading anything by an American ‘science writer’ (the one in question being described by Grant as ‘notorious’). Instead it is to pick up a point that Grant made about E.B. ‘Henry’ Ford (1901-1988) and his book Ecological Genetics. The later editions failed to mention a paper published in Science in 1968 which threw doubt on one of Kettlewell’s untested speculations. Grant’s students were said to be ‘disappointed that world-renowned scientists could so uncritically accept and promote untested hypotheses’.

The late Bryan Clarke (1932-2014) in his Biographical Memoir on Ford for the Royal Society wrote of the approach taken in Ecological Genetics:

It is written, of course, in his [Ford’s] wonderfully lucid style. It contains accounts of the researches that have already been described above, as well as those of his friends, colleagues and students…This was a galaxy of talent indeed, and a testimony to Henry's skill in choosing students and colleagues, but there were other galaxies that did not get a mention. The book was brilliantly and annoyingly parochial. Henry did not like mathematics, despite his friendship with Ronald Fisher, so that other theoreticians got short shrift. Nor did he like molecular biology, so that even in later editions of the book there was little about variation in proteins or DNA. Workers in the U.S.A. were largely ignored. One year before the last edition of Ecological Genetics, in 1974, R.C. Lewontin produced another brilliantly and annoyingly parochial book, The Genetic Basis of Evolutionary Change. The two works, both major events in the history of evolutionary writing, hardly shared a reference in common. But still Ecological Genetics, like its American counterpart, is necessary fare for serious workers in the field, still it is the clearest and least compromising statement of the 'selectionist' view, and still it is a joy to read.

My take is that Ford’s book (and, it would appear, Lewontin’s) followed the tradition of the book—and the major scientific review—as a personal statement on the subject in question, not just as an annotated bibliography with no conclusions drawn or personal view expressed. The purchaser of the book was buying the author’s considered opinion and the evidence that the author thought should get a mention. It was probably obvious to the highly eccentric Ford that the results of the experiments published in 1968 were deeply flawed. Should Ford have spent time describing and then dismissing that work? Or should he—as he obviously did—have simply ignored it?

I end with a question I argue about with myself. What should one do when discussing the dross—and there is a lot of it about—in published science? Spend time in minutely discussing why the authors (and the increasingly poor peer reviewers) were misguided, ill-read, incompetent or just stupid? Or simply ignore it, as many British scientists did in the 20th century on the genteel grounds of, if having nothing good to say, say nothing. The first approach might though be considered akin to taking sweets from children; the second construed as intellectual arrogance.

…and a final couple of words on Grant’s book and his pursuit for research on natural selection of Biston betularia across its entire range in the northern hemisphere: highly recommended.

Snakes’ Teeth: New light on their structure and evolution

As the dentist’s drill vibrated my teeth last week—and before being interrupted by the nurse being stung by a wasp (in Scotland in the middle of November)—I was thinking of a paper I had been reading on the teeth of snakes and the role of a particular component, plicidentine.

Plicidentine—a folded form of dentine—was found in the teeth of the snakes examined. Potentially it is present in all species of snake. Previously in extant reptiles it had only been found with any degree of certainty in some ‘varanoid’ lizards. The authors of the paper realised that the direction of the folding could explain how tubular fangs of venomous snakes have developed independently three times during the course of evolution. Tubular fangs are viewed developmentally as fully closed grooved fangs. The orientation of the folds in the plicidentine makes it easy to envisage that any one of the folds in non-venomous ancestors could have developed as a grooved fang involved in the delivery of venom.

A previous suggestion that plicidentine increases resistance to bending or compression during biting was examined in but biomechanical experiments provided no support for that view. Instead the authors suggest that plicidentine acts to improve the attachment of the long but shallowly rooted teeth to the underlying bone by providing an increased surface area. Since the teeth of ‘varanoid’ lizards are also relatively long and shallowly attached, the presence of plicidentine in these lizards as well as in snakes would fit the explanation proposed.

Palci A, LeBlanc ARH, Panagiotopoulou O, Cleuren SGC, Mehari Abraha H, Hutchinson MN, Evans AR, Caldwell MW, Lee MSY. 2021 Plicidentine and the repeated origins of snake venom fangs. Proceedings of the Royal Society B 288. 20211391. https://doi.org/10.1098/rspb.2021.1391 

Masai Mara Safari - 30 years ago: Cheetah with Four Cubs

 It would be difficult to imagine a better introduction to the Cheetah than this mother and four cubs we saw in the Masai Mara of Kenya in 1991. She had killed a Thomson's Gazelle and all five were eventually so full they could manage no more. And for physiologists a perfect example of gastric accommodation. Nothing looks more uncomfortable than a carnivore which has eaten so much that bursting seems the only possible outcome.

Edwin Ray Lankester: Gladly Making Fools Suffer

I have recently been reading a biography of Sir Edwin Ray Lankester (1847-1929). Most biologists never get to grips with the various mechanisms of evolution proposed or pursued in the six decades between Darwin and the Modern Synthesis. This was the era of comparative anatomy, a discipline which reigned triumphant in plotting the directions of evolutionary change and the relationships between organisms. Physiology was also making great progress but largely in isolation from comparative anatomy and evolutionary processes. Lankester, although a morphologist to the end, involved himself in both fields particularly as a young man. However, it is difficult to reconcile the enormous advances made by the comparative anatomists with the muddled thinking of how evolutionary change might occur propounded by those same individuals. Even while recognising the benefit of hindsight it is difficult not to conclude that many skilled anatomists with the ability to recognise homologous or analogous structures in other organisms simply could not get to grips with the implications of evolution or of natural selection. Some ideas propounded by well-established zoologists seem—and may have seemed at the time—nuts. It is for that reason that the era of Lankester is largely irrelevant to modern biologists. The twists and turns of evolutionary thought over the era fall firmly in the domain of the historians of science.

What many present-day biologists do not realise is that their immediate predecessors were brought up under a regimen of teaching the subject devised in the second half of the 19th century. One of the key players in that period was Lankester. The mix of lecture-style teaching with laboratory sessions in which ‘type’ specimens from major animal groups were dissected and drawn became the norm for around a century. 

Lankester was a man who did not mince his words, whether inveighing against the clerics who still ran Oxford or his nominal and clearly loathsome superior at the British Museum when the Natural History Museum, of which he was Director, was under its control. He walked away from a chair in Edinburgh after a few weeks when he found there was neither a lecture room or museum and that he would have to lecture throughout the whole year. He gave up this lucrative post (where the professor received the tuition fees) to return to his chair which had not been filled at University College, London. He gave the eugenics movement a mauling on the grounds its proponents were not distinguishing between the effects, in modern terms, of the genotype and the environment on the phenotype of the poor who they wished to stop breeding.

Lankester was a giant in British science, as practitioner, protagonist, promoter of new organisations, propagandist and populariser. He had interesting friends, Karl Marx, H.G. Wells and Anna Pavlova being notable examples, and many enemies. He had a rather sad personal life. Although there is some information on Lankester in books on other people and online (some of it inaccurate or misinterpreted) I had not read a proper biography. For such an important figure I was surprised to find that only one had been written. Few copies can have been printed because I had difficulty finding one to buy.

The biography, E. Ray Lankester and the Making of British Biology was published as a British Society for the History of Science Monograph in 1995. The history of its publication is interesting. Lankester’s papers were preserved by a niece. The author of the draft of the biography, Joseph Lester, contacted the niece in the 1950s. Eventually he was given access with the proviso that he would write an ‘approved’ biography. Initially the family had refused any access because Lankester was, in his time, a controversial figure. Lester worked on the biography in the 1950s and 1960s but could not find a publisher. He was an amateur—a reviewer of the book stated that he was a schoolteacher in Manchester and in his 90s at the time of publication—without the right contacts. Professor Peter Bowler FBA, a proper historian with interest in Lankester and his era of biological science, persuaded Lester that the only way his work would be published would be for it to be edited by a professional. Bowler, after reading the manuscript, decided to tackle the  job himself. He paid particular attention to the footnotes and to interpreting some of passages in the light of current knowledge. The title page therefore contains Lester as author and Bowler as editor.

The famous line about Lankester was written by his hero, Thomas Henry Huxley (under posthumous attack at present by the witchsniffers). Lankester need to work for his living and he felt his position at University College London had become precarious as student numbers and, therefore, income, fell. He wondered whether to apply for the job of Assistant Secretary at the British Association. Huxley dissuaded him:

Looking at things solely from the point of view of your interests, I should advise you against taking it—even if it were offered. My pet aphorism, ‘Suffer fools gladly’, should be the guide of the Assistant Secretary—You do not suffer fools gladly; on the contrary, you gladly make fools suffer.

….and having read about Lankester I have just remembered that in the final year at school for the Scholarship Level paper taken in addition to the ‘A’ Level papers I was asked to write about the body cavities and their origins. All that stuff about the coelom and in which phyla it is present came flooding back. It was Lankester who sorted it all out. Oh, and we were told that some examiners liked the blood to be referred to as a tissue, not just as a fluid. Lankester again.

I will though end with a quote from Lankester himself:

Science is no handmaiden, but in reality the master—the master who must be obeyed. The sooner and more thoroughly the people recognise the fact—and insist upon its acceptance in practice by tis representatives and governors—the better for them and their posterity.

Amen to that.

Ray Lankester by Leslie Ward, Vanity Fair 1905
The caption read::

”His religion is the worship of all sorts of winged and finny freaks"

Lester J. 1995. E. Ray Lankester and the Making of British Biology. Edited by PJ Bowler. British Society for the History of Science Monograph. ISBN 0-906450-11-X

This following obituary notice is rarely quoted because it is not picked up by internet searches, being buried in Proceedings of the Royal Society under a general title: Goodrich ES. 1930. Edwin Ray Lankester—1847-1929. Proceedings of the Royal Society B 106, ix-xv.

ZOO LIFE: ZSL’s Post-War Magazine 1946-1957

Zoo Life was a magazine published by the Zoological Society of London from 1946 until 1957. It was very different from its predecessor that had ceased publication in 1941 as wartime paper shortage made it impossible to continue. The pre-war magazine was a joint venture between ZSL and Odhams Press. It crammed an enormous amount of information, factual as well as anthropomorphic animal fiction, into its pages over the three years it was published under three titles, ending its run as Animal & Zoo Magazine.

Zoo Life was a far more sober affair. It was launched with the Spring issue of 1946. The first Honorary Editor was Edward Hindle FRS. He had become Scientific Director of the Zoo in 1944, vacating the regius chair in Glasgow which he had occupied for nine years.

The first page of the first issue contains the following editorial:

The Zoological Society of London has great pleasure in presenting to its Fellows and all other friends, a new publication which will be devoted mainly to illustrated descriptions of animals likely to be seen when visiting Regent’s Park or Whipsnade. The main features of each issue will be an article on some animal of special interest, because of its rarity or novelty, with a photographic illustration; a series of photographic studies; and an illustrated report on recent additions to the collection. Besides these attempts to portray some of the beauties of animal life, which should appeal to everyone, readers will also find vivid descriptions of the ways and manners of Zoo Life. 

Anybody coming across the early issues of Zoo Life will be struck by the quality of the artwork for the front covers. Many were available to subscribers as prints and may have been included with each issue since I found a number enclosed in a batch I have bought on eBay a few years ago.

The cover of the first issue was of a Markhor (Capra falconeri), reproduced from an original painting by the famous artist Joseph Wolf (1820–1899) around 1865 and held in the Society’s collection.

The first article was written by the former superintendent of London Zoo, Reginald Innes Pocock FRS (1863-1947). It was on the Okapi and gives far more information on its discovery than finds its way into modern accounts. A regular features was on happenings at London Zoo. The first was  particularly interesting because it described how the Zoo was trying to recover from the war years. One snippet from the war years was the arrival of a Coyote, brought from the USA in a bomber as a mascot by its crew and swiftly impounded as a potential carrier of rabies.

Finally, there is a reminder of the pre-war magazine. One of the articles—on play in animals at the Zoo (i.e. ‘behavioural enrichment’ in modern jargon) was by Craven Hill. He was the Evening Standard’s Zoo Correspondent at a time when all the major newspapers had such a designated position to follow the goings-on at Regent’s Park.

THE SEALS AND THE SCIENTISTS. A 1979 Book About an Important Study in 1950 on Lactation and Growth in the Grey Seal

Around 4 o’clock on days he was in Amo¹ with cigar burning brightly in his hand would wander into the coffee room for tea and regale us with stories of his exploits, of his enemies and of his mishaps. Several were about his work on seals on Ramsey, an island off the Welsh coast, in the late 1940s to early 1950s. Amo and his colleagues were the first to study the growth of the young seal in relation to the transfer of nutrients from the fat reserves of the mother. During a period of a few weeks when the pup grows from around 14 kg to over 50 kg the mother does not feed. All the pup’s growth and energy expenditure comes from the mother’s reserves. As one grows, the other shrinks. The fat-rich milk (1½ times the concentration in double cream) can only be described as having the consistency of emulsion paint with the smell of none too fresh fish. (For anybody contemplating working on pinniped milk my advice is not to use a mouth pipette; take it from one who knows.)

The take home message from the study was that about half the loss of weight of the mother manifests itself as growth of the pup. The other half fuels the mother’s and the pup’s energy requirements. However, having got that bit over most of Amo’s stories involved interactions with the locals who were utterly mystified by the comings and goings of these strangers to the offshore island.

What I did not know when I left in 1978—and have only recently discovered—was that an account of the work on the seals and on the scientists who took part was published by Leonard ‘Leo’ Harrison Matthews², his principal collaborator. The book, The Seals and the Scientists, appeared in 1979 (London: Peter Owen). It covers other studies on seals around the British coast and is beautifully written in a style that has long died out. One can almost see Matthews wearing his cape and carrying his swordstick on a trip to the publisher.

Matthews explained how the idea of penning a mother seal in a weighable cage on or near the beach and then weighing both mother and pup, while also taking milk samples, came about:

Professor Amoroso was sitting with me beside the fire in my study at Bristol one stormy winter evening in 1949. We were enjoying biological gossip over a jorum of hot rum and after discussing some puzzling things I had found in the insides of Basking sharks I had cut up with Gavin Maxwell on the island of Soay off the coast of Skye, the talk came round to the seals I had been studying in west Wales. He was Professor of Physiology at the Royal Veterinary College in London and was used to handling many kinds of strange animals, but had never had any dealings with seals.

After preliminary trips with various people interested in seals and decisions made on what was needed, the heavy equipment was made in Amo’s department’s workshop. Matthews described the party:

In the end only some of those who were interested in the seals could go with the Professor and me — Gwen Halley³, his brightest research student, Dolly⁴ [Matthews’s wife], Jean⁵ (Matthews’s daughter) and Allen Goffin⁶…Allen was the Professor’s head laboratory technician, section cutter, photomicrographer, mechanic and general standby; he had been in the Commandos during the war and was the strong man of the party— he could turn his hand to anything from cooking a splendid meal or humping a hundredweight of gear up an almost vertical cliff, to fixing and preserving the most delicate histological material.

They also had considerable help from Peter Rowe, the son of the local farmer.

The whole study was dubbed Operation LACTRAM—the investigation of LACTation in the Grey Seal at RAMsey. However, because the mother seal was named ‘Mrs Mopp’ after the  charwoman character in the radio programme ITMA, the whole affair is referred to as the Mrs Mopp Expedition. Her pup was named ‘Willie’.

The book has photographs of the Mrs Mopp expedition. They were extracted from a ciné film taken I suspect by Allen Goffin who amongst the many attributes listed by Matthews was a good man at ciné and still photography. I have been unable to find what happened to the film. It was shown at a meeting of the Physiological Society in November 1950, only around a month after the party left Ramsey, but it appears not to be held by the BFI (where another of Goffin’s films is archived). Does anybody know if it has survived?

Mrs Mopp and Willie were captured 3 days after parturition and kept in a large cage which could be weighed. When they were released 15 days later the mother went to sea and the party departed. Peter Rowe then noted that  the mother returned to feed the pup regularly for another 3 days and then left him to his own devices. 

The book ends with what happened a year later. Amo and Matthews were again on Ramsey. They had packed their equipment in October 1951 and were on the beach when Matthews decided to demonstrate his ability to ‘call’ out the cows from the sea. He succeeded in doing so but Amo sneezed and they retreated. However, they and the other scientists with them noticed that one of the cows hadn’t seemed bothered by human scent. Then Matthews saw the distinctive scars on her back. It was Mrs Mopp.

That ending though was not Amo’s most memorable story of their work on Ramsey. Amo realised that to get milk samples, a breast pump of the type used by human mothers was needed. As he said, a medical graduate and possessor of that ancient degree, Bachelor of the Art of Obstetrics (BAO) which Dublin awarded alongside its degrees in medicine and surgery, should have anticipated such a requirement. The comings and goings of the scientists visiting Ramsey were the talk of the small town on the mainland from which they obtained supplies. There were—shock horror—women with the men and one of those men, Amo, was black—and in 1950, Amo was the only black man they had ever seen. What was going on? Tongues were wagging when one of the party went ashore asking where he could buy a breast pump. Mission accomplished, the purchaser heard the gossip as he passed by: ‘Looking for a breast pump (the word ‘breast’ would have been whispered) he was. One of them must have had a baby’.

A final swig of tea and a long puff of the cigar, by now diminished in length, and Amo was across the corridor and back in his tiny office.

1 Professor Emmanuel Ciprian Amoroso CBE FRS (1957) 1901-1982.

2 Leonard Harrison Matthews FRS (1954) 1901-1986.

3 Gwen Halley went on to become lecturer in embryology at the then new Bristol vet school; I have no later information.

4 née Dorothy Hélène Harris 1901-1997.

5 Jean Dorothy Matthews, later Trewhella 1929-2021.

6 I am fairly sure that Allen Goffin was Alan Richard Goffin 1920-1984.

The Omnivorous Lizards of Aruba, or: Breakfast at home is never quite the same

Arriving at a hotel at around 3 am with a bad cold is not conducive to the best of tempers. And having got up to catch breakfast the next morning and then having to walk back to the room to collect the wodge of vouchers for different items of breakfast (a bizarre practice never seen before or since) that had been thrust into my hand at check-in, that temper was not improving. Eventually we emerged holding trays as if we were at an American student cafeteria and found a table on the deck close to the beach. We were on the Dutch island of Aruba, off the coast of Venezuela, in October 2002 on our way back to UK from Peru. The KLM flight stopped there to refuel on its way to Amsterdam and a few days of doing nothing before flying on seemed a good plan.

The almost entirely American clientele of the hotel had finished their breakfasts by the time we sat down. Inevitably, each table had been left with piles of uneaten food. That was being made short work of by hungry birds, Carib Grackles (Quiscalus lugubris), Eared Doves (Zenaida auriculata) and Bananaquits (Coereba flaveola). As the tables were cleared, only the sachets of sugar and artificial sweetener were left on the tables. The Bananaquits lifted each sachet in turn until they found one containing sugar. That sachet was then hauled onto a flat surface and pecked until the granulated sugar could be eaten. The day was improving and the champagne (obtained by a special voucher) in the full breakfast booked by our travel agent may well have helped.

Looking downwards we realised that food dropped on the floor by messy human eaters or by the birds was not going to waste. There was a whole squad of Common Iguanas (I. iguana) of all sizes as well as whiptails or racerunners (Cnemidophorus) I had to look up later; they were C. arubensis, as the name implies endemic to the island. Now the day was taking a very different turn and a morning catching up on sleep completed the job.

Male Aruba Whiptail eating melon

The start of each day followed the same pattern with the iguanas in particular hanging around occupied tables in the hope of handouts. The iguanas would eat pretty well anything offered; the whiptails preferred fruit but were not averse to small pieces of bread or bacon. One morning I took some video. These were the days of ‘standard definition video’ on miniDV tape with no stabilisation of the image.

Common Iguanas are well known omnivores. The Field Guide to the Amphibians and Reptiles of Aruba, Curaçao and Bonaire published in 2005 states that the whiptails on the islands are mainly herbivorous and noted ‘These island whiptails also eat insects and other arthropods and will eat carrion; they gorge on practically all other food which they can find around houses’.

With all I have written in the past few weeks about the colons of omnivorous lizards, the obvious question is does C. arubensis has ‘caecal valves’ as is well documented in I. iguana? 

Buurt G van. 2005. The Field Guide to the Amphibians and Reptiles of Aruba, Curaçao and Bonaire. Frankfurt: Chimaira.

Omnivory in the Italian Wall Lizard and Changes in Gut Structure and Function: The Results of a Translocation Experiment

My recent article on fruit-eating Italian Wall Lizards (Podarcis siculus) turned up an intriguing story about this lizard. In 1971 five pairs of this species were introduced onto the Croatian islet of Pod Mrčaru from a nearby islet, Pod Kopište, in the Adriatic Sea. Since that time the population has been studied intensively because, it was found, those on Pod Mrčaru ate far more plant material than those on Pod Kopište. Thirty-six years after the population was introduced plant material comprised 34% in spring and 60% in summer of the stomach contents, compared with 7% and 4% in the lizards of the original population.

Associated with that change in diet were a number of morphological changes. The heads were bigger and the bite force greater in the omnivorous lizards on Pod Mrčaru, changes attributed to the need to tear up plant material before swallowing. Particularly interesting to me was the finding of ‘caecal valves’ in the large intestine. In herbivorous lizards these structures are present and appear to impede the passage of digesta and thereby provide a fermentation chamber for the digestion of cellulose by micro-organisms. Nematodes were present in the gut of the omnivorous population suggesting they were ingesting the digested plant material.

The authors of this first study, published in 2008, were, in my opinion, unwise in appearing to favour the view that these changes within a species were caused by natural selection over a period of a few generations and were therefore an evolutionary event with a change in gene frequency akin to that seen in, say, industrial melanism in moths. The alternative but not mutually exclusive explanation is that lizards of this species have sufficient individual plasticity to respond in the way that they have to the ingestion of plant material. A paper published in 2010 by a largely different group not only extended the original observations but also obtained evidence that plasticity is the more likely explanation for the changes observed in the digestive system

A key experiment was of course to reverse the availability of plants in the diet. Genetically determined adaptations would not be reversed by a return to carnivory within a lifetime while adaptation brought about by a plastic response to the diet would be expected to lead to reversion. This experiment was done by the second group of researchers. Lizards from the introduced, omnivorous, were fed exclusively on arthropods for 15 weeks. One characteristic of the omnivorous lizards was a heavier and longer large intestine. In the arthropod-fed group, the size of the large intestine was smaller. Furthermore, there was no sign of a caecal valve in any of the 20 animals that had been fed exclusively on arthropods.

The second group of authors also cast doubt on whether the larger heads and bite strength of the lizards on Pod Mrčaru are directly related to their plant-rich diet. The greater population density of the lizards on Pod Mrčaru compared with Pod Kopište may have resulted in selection for greater ability for physical combat. That selection pressure rather than that from the tearing of plant material may have lead to the larger body sizes, the more robust heads and the greater bite force observed in the Pod Mrčaru lizards

While a mixture of selection and plasticity may explain the overall changes in the lizards on Pod Mrčaru, it does seem likely that with respect to the digestive system the changes are the result of plasticity not selection. This conclusion does not mean to say that in other species of lizard which are largely herbivorous the presence of a large colon containing a number of caecal valves is not genetically determined.

Worth noting here is the fact that the Wikipedia article on this lizard is misleading—as is so often the case on herpetological matters—and does not take into account later findings on the lizards of Pod Mrčaru.

If there are—as does seem to be the case—species of lizards that can change to a more herbivorous diet, develop the morphological and biochemical features necessary to digest plant material and absorb the nutrients produced in a reversible manner then three questions arise. The first is why the lizards introduced to Pod Mrčaru began to eat a larger proportion of plant material. Was it because the competition for food resources in the form of small invertebrates became intense as the population grew? The second question is the reversible mechanism by which the colon forms caecal valves.

Looking at photographs of the caecal valves in P. siculus and at those from other, mainly herbivorous species, it appears that the valve comprises a transverse infolding of the wall of the colon. It is relatively easy to envisage an area of localised cell division and development of a ridge which narrows the lumen. In reverse, local loss of cells would flatten the infolding. For those physiologists and cell biologists working on local signalling mechanisms in the intestine P. siculus is not without interest. Incidentally, research over the past forty years has shown the alimentary canal of reptiles to be highly labile in response to changes in food intake; far more so than would have seemed imaginable.

Later work, published in 2020, in again comparing the lizards on the two islets have not been so clear cut but do support plasticity as the explanation. I have some qualms about the methodology and the lack on information on the actual absorption of nutrients from the gut as opposed to concentrations found therein. However there was clear evidence that in 2013 no lizards were found on Pod Mrčaru with caecal (also known as hindgut) valves. The reason for that shift over time can be debated but these findings strongly support the view that the induction of enzyme and nutrient transport systems as well as the growth of caecal valves are part of the result of plasticity within an individual rather than the outcome of a process of natural selection.

The third question is whether lizards of this species turned to an omnivorous or largely herbivorous diet elsewhere in their large range. The current field guide to European reptiles describes Podarcis siculus as ‘an opportunistic feeder, taking a variety of invertebrates and plant matter’. The sort of response that given current knowledge would be expected could very much depend on the type of plant food being eaten. There is a world of difference in the sort of chemical digestion and nutrient absorption needed to process sugar-rich fruit, as in the grape-eating lizards from mainland Italy that made their way accidentally to UK, and other plant materials for which the digestion of cellulose by microorganisms is necessary.

The opportunistic nature of Italian Wall Lizards can be seen in the following photographs sent to me by a regular reader of these articles, David Lambert. They were taken at Punta del Capo, a small flat-topped rocky promontory near Sorrento. The lizards proved very willing to share a picnic  and his photographs show them eating banana, tomato and bread.

David Lambert's photograph of an Italian Wall Lizard eating bread

...and banana

...and tomato

The location of the islets in the Adriatic
From Wehrle et al 2020

In chronological order:

Herrel A, Huyghe K, Vanhooydonck B, Backeljau T, Breugelmans K, Grbac I, Van Damme R, Irschick DJ. 2008. Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proceedings of the National Academy of Sciences of the USA 105, 4792-4795 doi10.1073/pnas.0711998105 

Vervust B, Pafilis P, Valakos ED, Van Damme R. 2010. Anatomical and physiological changes associated with a recent dietary shift in the lizard Podarcis sicula. Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches 83, 632-642 doi.org/10.1086/651704

Wehrle BA, Herrel A,  Nguyen-Phuc B-Q, Maldonado  S,  Dang RK, Agnihotri R, Tadić Z, German DP. 2020. Rapid dietary shift in Podarcis siculus resulted in localized changes in gut function. Physiological and Biochemical Zoology 93, 396–415. DOI: 10.1086/709848