William Harvey and the Circulation of the Blood. Learn how science is done from a classic film

First-year students confined to their living quarters and online teaching by the resurgence of covid-19 would do well to watch the film, William Harvey and the Circulation of the Blood. This classic, filmed in 1971-72 for the Royal College of Physicians, was itself a third remake of the same title; the original version was made in 1928 to celebrate the publication of Harvey’s De Motu Cordis three hundred years earlier with another version in 1957 for the tercentenary of Harvey’s death. The history of the three versions is explained in the third version, with the first being the idea of Sir Thomas Lewis FRS (1881-1945) and Sir Henry Dale FRS (1875-1968).

In overthrowing the teachings of the ancient anatomists he had been fed while studying at the University of Padua, William Harvey established the circulation of the blood and the working of the heart not simply by positing from anatomical observations but by experiment. But, as the film shows, he used ways of thought that are still essential for knowledge to advance today.

The student or anybody else watching this film learns the importance of:

• Experiments that are simple, direct and, therefore, elegant
• The value of taking a comparative approach—gaining knowledge from a variety of organisms in order to test a generality
• Armchair physiology—using simple quantitative data to test competing hypotheses
• Using a mechanical analogy—the heart as a fire engine pump is an example
• Knowing the  historical literature in detail
• Travel to see and hear current thinking in different centres of excellence

The full version can be found HERE on the Wellcome Foundation website. The Wellcome provided the financial support needed to make the film. There are somewhat shorter versions also online but the few extra minutes are well worth watching.

William Harvey was a great scientist before the word was invented and a true exponent of Nullius in Verba thirty years before the Royal Society was founded.

The film was directed, produced and photographed by Douglas Fisher FRPS for the Royal College of Physicians. Douglas Fisher had made films for the Wellcome Foundation and is remembered for his filming for Granada Television’s Zoo Time in the 1950s, and for his later wildlife films.

The writers and researchers for this version were the historian Gweneth Whitteridge (1910-1993), Charles Edward Newman FRCP (1900-1989) and Leonard Maslin Payne (1911-2000), Librarian at the Royal College of Physicians. Harvey’s experiments were reconstructed by Michael de Burgh Daly (1922-2002) who was Professor of Physiology at St. Bartholomew's Hospital medical school and Leonard George Goodwin FRS (1915-2008) then Director of Science at the Zoological Society of London. Len Goodwin also read the words of William Harvey, translated from the Latin, for the soundtrack.

Quaint and redolent of instructional films of the middle decades of the 20th century, this classic is now nearly 50 years old. Shall we see fourth version, this time using video and computer graphic simulations, for the 400th anniversary of De Motu Cordis in 2028?

Japanese ‘Snow’ Monkeys. After bathing in a hot spring, how much heat do they lose?

In the days before central heating who can remember having to get out of a warm bath into the cold air of a bathroom in winter? It was a case of getting dry and into clothes as quickly as possible. That thought never left me as I watched the Japanese Macaques (Macaca fuscata) sitting for several hours at a time in the hot spring of Jigokudani Monkey Park in Nagano, Japan. I was reminded again when I looked through the video and photographs we had taken in 2009. We wondered at first if the thick coats of these monkeys did not wet easily and water therefore did not penetrate to the skin. However, we saw—and this can be seen in the video where there is grooming going on—that their coat is absolutely saturated. They really do get soaked to the skin.

In the depths of the Japanese winter it is easy to see that monkeys would save a considerable amount of energy needed to keep warm by sitting in volcanically warmed hot spring or onsen for part of the day. But even with a good shake after emerging from their soak in the onsen, there seemed a lot of water left to evaporate and therefore cool the body in air temperatures well below freezing.

Regardless of the length of time in the water, the cost of keeping the body warm after coming out into the cold air in terms of energy consumption would be the same. Therefore, in order to ensure that the bathing experience does not result in a net energy loss, one might expect that monkeys would stay in the hot water for relatively long periods, and that is what they do. Some sit, sometimes with their eyes closed, with their heads on a surrounding rock; others groom or are groomed while some dive to the bottom to retrieve grains of corn (which looked like wheat) that are scattered throughout the park during the day.

While I have seen research on thermoregulation in Japanese monkeys I have seen no studies or calculations on their energy balance as a result of their getting warm in onsen and then getting out with saturated thick fur, although potential problem was raised in the 1970s. The question is important because of the demonstration that the conception rate of females is higher in those with higher energy reserves and body fat. Any mechanism to reduce energy expenditure in the cold will be of advantage so there must be some sort of balance being achieved between time spent foraging and time spent immersed in hot water—and of course the downside of emerging sodden into cold air. I have been unable to find out if bathing is related to supplementary feeding in the park. A well-fed monkey that does not have to forage for so long could be one that can take time out in an onsen and thus help its energy balance.

The importance of bodily condition for reproduction in female Japanese Macaques is apparently reflected in the use of the onsen: it is mainly dominant females (who defend the pool) and they pass the habit to their daughters. Subordinate females rarely get the chance. Some adult females spend up to 10 hours in the water and some have been seen to stay there overnight. The young (who would get even colder with their relatively large surface area after emerging sodden) rarely enter the water voluntarily, although as the last sequence in the video shows, do sometimes get very wet when trying to reach their mothers in the pool.

The bathing behaviour is said to have been first seen in the early 1960s with a female immersing itself to reach some floating beans. I have not been able to find out whether bathing is confined to the one troupe which, as I noted above, receives supplementary food, or if the behaviour has been observed elsewhere where the range of the monkeys and hot springs coincide.

Here is the video from 2009:

Garcia C, Huffman MA, Shimizu K, Speakman JR. 2011. Energetic consequences of seasonal breeding in female Japanese Macaques (Macaca fuscata). American Journal of Physical Anthropology 146, 161-170.

Zhang P, Watanabe K, Eishi T. 2007. The habit of hot-spring bath in a free ranging group of Japanese macaque in the Jigokudani, Nagano Prefecture. American Journal of Primatology 69, 1425-1430.

Edward Bles (1864-1926). Part 2. Gentleman zoologist. Frogs, plankton, embryos and protozoa

Edward Bles was a zoologist with a substantial private income. He did not need to work but did so anyway, eventually in his own private laboratory. As described in Part 1 he was the first to describe the development of Xenopus in detail. Indeed much of his his work was in embryology at a time when this field was a leading and often controversial aspect of zoological research. Confusing for genealogists, he was known as Edward Jeremiah Bles but his birth was registered as Jeremiah Edward. Therefore, some documents do not fall immediately to hand when searching the historical records.

Bles was born in Salford near Manchester in 1864, the son of Abraham Jeremiah Samuel Bles (1838-1909) and Esther Polak. Abraham and his brother, David Samuel, were born in The Hague; their father established S.D. Bles & Co, merchants and shippers, in Machester largely for the Dutch trade. The Bles’s were leading lights in the Jewish community in Manchester as well as looking after the interests of the Dutch. Abraham was Dutch Consul.

In 1876 the Manchester Courier reported that young Bles had passed the Government Science Examination. Aged 14, Edward Bles was sent to a school in Hanover and at 18 started work in the family business. An interest in science which developed at school in Germany led to his joining the Manchester Microscopical Society (still in existence) of which he became Secretary. Such clubs brought amateurs and professionals together and it was there that Bles fell under the influence of Arthur Milnes Marshall FRS (1852-1893) who, in 1879 at the age of 27 had been appointed to the new chair of zoology in Owens College (later incorporated into what is now the University of Manchester). Bles therefore became a student at the college. In 1890 Bles published with Marshall papers on the development of amphibians, in this case the kidneys and fat bodies, and the blood vessels.

From Owens College, he moved to King’s College, London, graduating with a B.Sc in 1890. His obituarist (see below) noted that he spent time at the Naples marine laboratory but returned to Manchester, as junior demonstrator in zoology. In the summer of 1892 he was working at the Plymouth laboratory of the Marine Biological Association on plankton. He is shown in the resulting paper as honorary research fellow at Owens College. Bles must have been well known in the Plymouth laboratory because he was appointed Director in April 1893. But this was at a time of financial stringency. The Director had a heavy administrative load which prevented personal research. These factors resulted in a rapid turnover of Directors. Bles left in 1894. However, there may have been other reasons. In his second report as Director he noted that the issue of the Association’s journal was late: ‘Unforeseen circumstances affecting myself have caused a further postponement’. Were these ‘unforeseen circumstances’ and leaving Plymouth related to illness, which dogged him in later years, or to the fact that he married Bertha Bachmann of Augsberg in Dusseldorf, Germany on 12 November 1893?

October 1896 saw him admitted to King’s College, Cambridge at the age of 32. He graduated B.A. (as a research degree—the Ph.D, ‘the German degree’ was not awarded in Cambridge until 1921) in 1898 (M.A. 1907). In 1902 John Graham Kerr left Cambridge to the chair of natural history in Glasgow taking Bles (and his frogs) with him as senior assistant, which would be the equivalent of senior lecturer in English universities.

After 5 years in Glasgow, by which time he had been awarded the D.Sc. degree (by the University of London in 1906) and elected to the Royal Society of Edinburgh in 1904, Bles moved out of academia. First he moved to the Hill House, Iffley, Oxford and then to Cambridge where he and Bertha lived at ‘Elterholm’, 12 Madingley Road—a very large house. It would appear it was there that he further equipped his laboratory and ‘started to breed various species of rare amphibia, a difficult enterprise in which he had the assistance of his devoted wife’.

By that time he was also working on Arcella, a freshwater protozoan, in particular the role and control of the gas vacuoles which regulate its buoyancy. Bles had a marked determination not to rush into print. Although he had virtually completed the work by 1914, his long paper was not published until after his ‘very sudden’ death on 3 May 1926. Bertha, who died in 1960, had again helped Bles with is research and she helped with publication. Over the years it has been widely cited. He had again commissioned Kirkpatrick Maxwell to draw the plates.

One of the plates from Bles's paper
on Arcella which was published
three years aftere hisa death

Here is Bles’s words is a description of a part of this work:

These uniformly positive results strongly support the view, which has long been held, that the function of the gas-vacuoles is to reduce the specific gravity of the Arcella, and float it up to the surface which is rich in dissolved oxygen. But it is now possible to go a step farther. In considering the natural causes, or changes in the environment, which might possibly stimulate gas formation for hydrostatic purposes in Arcella, the first consideration was, what is the most obvious and most important physiological difference between the water at the bottom and the water under the surface-film? This is clearly a difference in oxygen pressure. The analyses of pond-water for the determination of dissolved gases carried out by Knauthe (1898, 1899) and Zuntz (1900) show that pond-water may, by the influence of physical and biological conditions, be entirely deprived of oxygen. Owing to the slow rate of diffusion of oxygen in water, the bottom water of a pond or ditch, exhausted of oxygen, will be replenished only a long time after the surface layers. Hence it will clearly benefit those aerobic or semi-anaerobic organisms which live on the bottom, to have a means of escape which will rapidly carry them from a level of oxygen depletion to a level of oxygen plenty. The principal stimulus to form gas-vacuoles in Arcella and similar organisms which live at the bottom of ponds and ditches, is lack of oxygen. There may be, and probably are, other sets of external conditions which stimulate the production of gas by these organisms, and there are also conditions arising within the cell which stimulate the gas-forming structures. These will be described and discussed later…

It is evident that in Cambridge Bles was well known and respected. Sir Frederick Gowland Hopkins (1861-1947) wrote Bles’s obituary for Nature while he and David Keilin (1887-1963) completed the Arcella paper, the biochemical aspects of which fell into their own interests in cell metabolism.

Hopkins began the obituary in Nature:

By the recent death of Edward J. Bles, zoological science has lost a devoted worker whose qualities of mind and character were of the highest. It is the faith of many of his friends that, but for factors of temperament, and health, he would have become a leader of thought in the subject of his choice. His publications, though of high merit, were relatively few; but his intimates know that they were far from representing all that he accomplished, and are aware of the temperamental restraints but for which he could and would have published much more. He was one of those investigators-deserving sympathy from colleagues with easier standards—who would fain allow publication to wait for perfection, and yet realise even better than others that perfection never arrives. In spite of such inhibitions, or perhaps because of them, his published output is of high value and stamped with the quality of absolute reliability.      For elementary teaching, or, at any rate, for the shackles of departmental teaching and organisation, Bles had some distaste. On the other hand, he was the ideal colleague and one of the most educative influences for the young research worker…

He ended:

Bles was not merely a scholarly biologist in a very wide sense, he was also a man of fine general culture; music, literature, and the arts all made a vivid appeal to him. He had, moreover, a true sense of values and a very beautiful appreciation of the relative importance of things. His knowledge was of the widest, but so philosophic was the cast of his mind that synthetic thought was essential to him. He endeavoured always to see things as a whole. 

I have tried to draw up a list of Bles’s publications; it is shown below.

Bles’s legacy extends beyond his publications. He left the entire residue of his estate (about £44,000) plus his equipment and books to the University of Cambridge. It is difficult to equate the worth of that amount of money to today’s economy but in terms of income value (using GDP/capita as the index) it represents £13 million. Over the years, the Bles Fund has funded the Charles Darwin Chair of Animal Embryology—Bles’s express wish as was its use for ‘the promotion and furtherance of biology as a pure science’.

I have been unable to find a photograph of Edward Bles.

In the final part of this series I will return to Bles’s interest in amphibians and how he came to have a walk-on part in the Kammerer controversy.

Hopkins FG. 1926. Dr Edward J. Bles. Nature 118, 90-91.

Publication by Edward J. Bles (Jeremiah Edward Bles):

Bles EJ. 1884. The remarkable sunsets. Nature 29, 427-428.

Marshall AM, Bles EJ. 1890. The Development of the Kidneys and Fat Bodies in the Frog. Studies from the Biological Laboratories of Owens College 2,133-158 plus 1 plate.

Marshall AM, Bles EJ. 1890. The Development of the Blood-Vessels in the Frog. Studies from the Biological Laboratories of Owens College 2,185-268 plus 3 plates.

Bles EJ. 1892. Notes on the plankton observed at Plymouth during June, July, August and September 1892. Journal of the Marine Biological Association of the United Kingdom 2, 340-343.

Bles EJ. 1893. Director’s Report,—No. I. Journal of the Marine Biological Association of the United Kingdom 3, ix-x.

Bles EJ. 1894. Director’s Report,—No. II. Journal of the Marine Biological Association of the United Kingdom 3, xvii-xx.

Bles EJ. 1898. The correlated distribution of abdominal pores and nephrostomes in fishes. Journal of Anatomy and Physiology 32, 484-512.

Bles EJ. 1898. On the openings in the wall of the body-cavity of vertebrates. Proceedings of the Royal Society 62, 232-247.

Bles EJ. 1901. On the breeding habits of Xenopus laevis Daud. Proceedings of the Cambridge Philosophical Society 11, 220-222.

Bles EJ. 1905. The life-history of Xenopus laevis Daud. Transactions of the Royal Society of Edinburgh 41, 789-821.

Bles EJ. 1905. Notes on the development of Phyllomedusa hypochondrialis. Report of the 74th Meeting of the British Association for the Advancement of Science in 1904, pp 605-606.

Bles EJ. 1905. Bles E J On the hatching of anuran tadpoles and the function…[incomplete]. 6th International Congress of Zoology, Bern 1904. (Compte-rendu des séances du sixième Congrès international de zoologie, tenu à Berne du 14 au 16 août 1904[no further details]

Bles EJ. 1906. The life-history of Xenopus laevis Daud. DSc Thesis, University of London.

Bles EJ. 1907. Notes on anuran development: Paludicola, Hemisus and Phyllomedusa. In The Work of John Samuel Budgett, Balfour Student of the University of Cambridge. Edited by J. Graham Kerr, pp 443-458 plus 6 plates. Cambridge University Press.

Bles, EJ. 1929. Arcella. a study in cell physiology. Quarterly Journal of Microscopical Science 72, 527-648.

Comparative anatomy and physiology of excitatory conduction in the heart: Francis Davies and Eric Francis in Sheffield

‘Have you ever tied a Stannius ligature?’, is a conversation stopper. If the answer is ‘yes’ then you know the person you are talking to studied physiology at some time in the past and that a practical class was concerned with the workings of the frog’s heart—an organ ideal for hamfisted students since it beats spontaneously in isolation and they can learn a great deal about how hearts work in a couple of hours*. However, amphibian and reptilian hearts differ in a number of respects from those of birds and mammals.

One of the key players in the comparative anatomy and physiology of the heart is not remembered by the herpetologists, for example, although his great friend and collaborator is. Francis Davies (1897-1965) was at first sight a classical human anatomist—indeed he became co-editor of Gray’s Anatomy. He was born at Merthyr Tydfil, studied medicine in Cardiff and then University College London. In 1924 he became Senior Demonstrator in anatomy at UCl; he then moved to King’s College London as Reader. In 1935 he arrived in Sheffield as Professor; there he stayed until retirement in 1962. In Sheffield Davies worked on the heart with his friend, Eric Thomas Brazil Francis (1900-1993) who became Reader in Zoology until he retired in 1965.

Together, Davies and Francis studied the hearts of amphibians and reptiles in order to determine how the signal from the pacemaker that sets the heart rate passes first to the atria and then to the ventricle (single in amphibians and most reptiles) or ventricles (in crocodiles as in birds and mammals). Earlier in the 20th century Sir Thomas Lewis (1881-1945) had worked out what happened in mammals: specialised heart muscle cells form a dividing bundle of fibres (the Bundle of His) that convey the message to contract to all parts of the ventricles from the atrio-ventricular node. However, there are no special fibres from the pacemaking sino-atrial node to the atrio-ventricular node; impulses pass across the atria from muscle cell to muscle cell like a Mexican wave. It was Lewis’s brilliant work which made not only the physiology textbooks; the research explained a number of conditions that account for heart disease.

Conduction in the mammalian heart
The structures shown in BLACK are not present in
amphibians and reptiles.
from my 1961 edition of the classical physiology textbook
'BDS'

Francis had already published his book, The Anatomy of the Salamander, and their first joint work, published in 1941, was on the heart of that species (Salamandra salamandra). Francis and Davies concluded that in amphibians and reptiles there is no special conducting system in the heart responsible for spreading the process of excitation to the ventricles; the waves of excitation pass directly but relatively slowly from heart muscle cell to heart muscle cell. In other words, the Mexican wave of contraction continues across the whole heart in contrast to birds and mammals where a specialised bundle of fibres takes over.

Davies and Francis proposed that the reason for this major difference in the heart between ectothermic amphibians and reptiles, on the one hand, and endothermic birds and mammals on the other, is the the pace of life; heart rates are lower in the former than in the latter. Relying on a Mexican wave is just too slow for high heart rates to be achieved. They also suggested that the development of a special conducting system was a relatively recent evolutionary change. Their views still hold good.

But what about crocodilians with their two ventricles? Do they have a system like that in birds and mammals, or one characteristic of extant reptiles? Davies and Francis had that covered. They showed that crocodilians have no specialised conducting pathways.

Francis Davies and Eric Francis were not exemplars of the dyed-in-the-wool anatomists who never lifted their eyes from the dissecting table; nor did they confine their studies to comparative anatomy. Both stressed form and function. Davies while undoubtedly seen as a human anatomist of the old school, stressed in teaching anatomy to medical students ‘living’ functional anatomy. Francis was a zoological polymath. In their work on the vertebrate heart, they threw every technique then available at the problem of how excitation by the pacemaker is conducted to all parts: gross observation, dissection, serial sections for histology, histochemistry, slow-motion cinephotography, in-vitro physiology and electrocardiography.

Francis Davies had been unwell for some years when when he retired in 1962. He died in 1965. Eric Francis wrote his obituary for the Journal of Anatomy.

ETB Francis's drawing of the Salamander heart from the 1941 paper

*By tying two ligatures Hermann Friedrich Stannius (1808-1883) showed that the pacemaker of the frog’s heartbeat is in the sinus venosus and that impulses pass from there to the atria and then the ventricle. By isolating regions of the heart these two ligatures also showed that the chambers beat to their own rhythm spontaneously in the absence of input from the pacemaker. The first Stannius ligature is tied between the sinus venosus and the right atrium; the second between the atria and the ventricles. As a hoax the late Jim Linzell and I, in response to a letter asking for exhibits for a museum, put a length of cotton thread in an envelope and sent it along with the explanation that this was Stannius’s third ligature which he never got round to using because his wife had sent a message telling him to get home before his dinner got cold. It was dated 1 April. We never had a reply.

Davies F, Francis ETB. 1941. The heart of the salamander (Salamandra salamandra L.), with special reference to the conducting (connecting) system and its bearing on the phylogeny of  the conducting systems of mammalian and avian hearts. Philosophical Transactions of the Royal Society B 232, 99-130.

Davies F, Francis ETB. 1946. The conducting system of the vertebrate heart. Biological Reviews 21, 173-188

Davies F, Francis ETB, King TS. 1951. Electrocardiogram of the crocodilian heart. Nature 167, 146.

Davies F, Francis ETB, King TS. 1952. The conducting (connecting) system of the crocodilian heart. Journal of Anatomy 86, 152-161.

Francis, ETB. 1965. In memoriam: Francis Davies. Journal of Anatomy 99, 913-915.

Jensen B, Boukens BJD, Postma AV, Gunst QD, van den Hoff MJB, Moorman AFM, Wang T, Christoffels VM. 2012. Identifying the evolutionary building blocks of the cardiac conduction system. PLoS ONE 7(9): e44231. doi:10.1371/journal.pone.0044231 

Vole Population Crashes: Was there an attempt to suppress a ‘lamarckian’ hypothesis in the 1950s?

Field Vole or Short-tailed Vole
Photograph by Tim Melling

I apologise in advance for this post. In trying to find the answer to an allegation that a paper was suppressed because it proposed a controversial hypothesis, I have to skim the surface of a topic at the heart of ecology. It is a topic that has spilt over into the physiology of ‘stress’ and it is a topic that has been the subject of a great deal of mathematical modelling. I am dealing with just one aspect from a mainly historical perspective but it is an aspect that is at the centre of the problem of factors controlling animal populations and one which provoked an often bitter controversy. The question though is simple: how can fluctuations in the size of populations of voles from year to year be explained?

I knew little of the work of the Bureau of Animal Population which existed at Oxford from 1932 until 1967 under the leadership of Charles Elton¹. What I did know came first from my former colleague at Babraham, the late John Perry², who had been a member of the Bureau in the 1940s, and from his friend H.N. ‘Mick’ Southern³, another stalwart, when the three of us sat together at meetings of the old Zoological Club in the 1970s. Another member, John Clarke⁴, sometimes came to Society for Endocrinology meetings to describe his continuing work on the reproduction of voles. Before that I knew from gossip the battle that went on to bring the Bureau in the zoology department proper because In the mid-1960s interest in the goings on at Oxford was intense. Zoology at Oxford has a well-maintained reputation for internecine warfare and John Phillips⁵ returned to Hong Kong from a short visit to U.K. in 1966 full of stories he had heard of the troubles at Oxford occasioned by the eventually successful attempts of the head of department, J.W.S. Pringle⁶, who had arrived from Cambridge in 1961 determined to change things, to integrate the outlying units, into the zoology department.

A couple of years ago I found that Peter Crowcroft⁷ had written a book on the history of the Bureau, of which he was a former member. As I read it I came across what appeared to be a shocking example of scientific censorship in the early 1950s. I thus became acquainted with the world of voles and of Dennis Chitty⁸ who, after Oxford, was Professor of Zoology in the University of British Columbia. This is what Crowcroft wrote:

When Chitty had analyzed his data from the Lake Vyrnwy population [of the Field Vole, Microtus agrestis] that had been stud­ied continuously from 1936 through 1939, he found himself unable to explain their crash in terms of the classic factors: food, weather, preda­tion, and disease. He came to suppose that overcrowding and its asso­ciated social strife might have caused the high mortality among young voles born when numbers were highest. Adverse effects of overcrowding could also explain the reduced productivity of females subjected to it. That hypothesis would not have caused any raised eyebrows, even in the 1940s. The Lake Vymwy population continued to decline, however, in the next generation, when there was no longer an overcrowded vole society, and when food appeared to be abundant. Chitty felt obliged to offer, as the simplest possible explanation, the existence of an inherited disability: "During the time of their almost complete disappearance in 1938 or 1939 voles were not subjected to any known environmental conditions likely to have caused excessive mortality. The hypothesis is therefore advanced that death was primarily due to adverse conditions to which the parents were subjected in the previous breeding season."       

That suggestion not only caused the eyebrows of authorities in popu­lation matters to go up, it also raised the hairs on the backs of their necks. This smacked of the Lamarckian heresy! Chitty could not get the paper published in the journal of his choice. But Sir Alister Hardy read it objectively, and communicated it to the Royal Society for publication in their Transactions, a most prestigious place. 

Now ‘maternal effects’—an example of which Chitty proposed—are well-known phenomena in many different organisms. They are lamarckian in the sense that a mother (or a father through ‘paternal effects’) can affect the performance of her offspring by pathways not involving a difference in the genes (which would be really lamarckian). Maternal effects, in short, are a form of non-genetic inheritance†.

If what Crowcroft wrote was true, the editors of the journal to which Chitty’s paper was first submitted would indeed have been guilty of suppressing an inconvenient hypothesis. However, Crowcroft made several mistakes in describing Chitty’s work which made me wonder if he had got hold of the wrong end of the stick. The first error was that Sir Alister Hardy did not communicate the paper for publication by the Royal Society. The Fellow who did was the then Professor Peter Medawar⁹. The second was that Crowcroft seemed to confuse this hypothesis of Chitty’s, which involved a maternal effect, with his later hypothesis for the phenomenon of vole cycles which involved genetic selection at different stages of the population cycle. This replacement hypothesis, not the one for a maternal effect, has been termed the ‘Chitty Hypothesis’.

After I read this Crowcroft’s account I began to think that Chitty and the people around his lab (including Crowcroft) had interpreted rejection of his paper because the hypothesis he advanced to explain it was lamarckian, rather than for the multitude of other reasons editors reject papers or suggest parts be rewritten. Crowcroft’s book appeared in 1991. In 1996 Chitty himself wrote a book describing his virtually lifelong interest in the control of animal populations and the disappointments it had caused him.  Chitty made no mention of the paper being rejected because it contained an apparently lamarckian hypothesis but because he had dared to propose a hypothesis at all. He wrote of this episode:

The account of my prewar work would have appeared in the Journal of Ani­mal Ecology if Charles [Elton] and I had not stepped down as editors. But the new editor, H.C. Gilson, took a dim view of the paper and wanted it rewritten. Ten of the pages, he complained, seemed to be largely speculation. “Even if they were not, [he wrote] they would be too general in character to hang on to this paper.” His comments confirmed the doubts I held at the time about the danger of speculating, especially as they were followed by phases such as the following: “All this is mere vague speculation . . . these ex-cathedra statements . . . if you will read the paper critically . . . infuriating to the reader . . . would you make up your mind . . . such indifferent photographs . . . much of interest and value pokes out of the paper like gleams of sun­ shine in places.” 
     I was more than somewhat upset—more than I should have been…This is probably the way most young authors feel when one of their brainchilden has been thrown to the lions of peer review. So it was some time before I could look objectively at the contrast between what I’d writ­ten—“needless to say I shall very gratefully welcome all your criticisms”— and the lack of gratitude I felt when they landed on my desk. 

In short there seemed to be no mention of a particular hypothesis, only that the data did not justify the degree of speculation. Chitty went on to describe the rôle of Medawar in getting the paper published: ‘His opinion of the need to speculate (though not necessarily of how I did it) restored my self-confidence’.

The question remains: would Chitty’s paper rewritten on the lines suggested by the editor of Journal of Animal Ecology have made a better paper than that which appeared largely unchanged in Philosophical Transactions of the Royal Society. I thought I, a non-ecologist, should read it.  And so I did, several times, and found my sympathies lie, 70 years on, with the editor of Journal of Animal Ecology. The style of data presentation alone has changed greatly but even so the paper would have qualified for my late colleague’s description of ‘publishing the contents of his notebook’. However, ‘much of interest and value pokes out of the paper like gleams of sun­ shine in places’ as Gilson wrote. Perhaps Chitty should have grasped the nettle and re-written it in a less discursive style while aggregating the raw data into simpler tables with more statistical analysis. My guess is that Gilson*, as the new editor of Journal of Animal Ecology, was attempting to present ecology as a harder science with crisp analysis and presentation than that conveyed by the previous Elton/Chitty régime.

A fierce critic of Chitty’s interpretation of the data from Lake Vyrnwy was David Lack¹⁰, next door at the Edward Grey Institute of Field Ornithology. Lack was of the view that only three factors can control natural populations: disease; predators or parasites; food shortage. He did not accept that Chitty had eliminated the influence of these factors before producing a hypothesis that crowding and thus ‘strife’—in other words control entirely within the vole population itself—causes the fall in numbers. While Chitty defended his views vigorously, on reading his book I remained unconvinced that he had eliminated the rôle of ground predators like stoats and weasels or that tuberculosis, which was present, might have been more important in the population declines than the evidence then suggested.

If, on the other hand, the external factors of Lack really can be eliminated as an explanation, which Chitty continued to contend, and having read something of the recent thinking on explanations of cycles in vole populations, there seems to be the view that Chitty’s original idea of maternal effects brought on by crowding might provide the answer rather than his ‘Chitty Hypothesis’ based on changes in selection and gene frequency.

In conclusion, I have not been able to confirm Crowcroft’s view that Chitty’s paper was rejected by the editor of Journal of Animal Ecology because it ‘smacked of the lamarckian heresy’. It is true that rejection on those grounds could have been hidden in the criticism of ‘speculation’ but having read the paper I can see why the editor acted as he did; he may not have objected to a particular hypothesis but to any hypothesis being advanced from what he, or possibly a referee advising him, saw as incomplete or inadequate data.

Finally, Lake Vrnwy, an artificial reservoir in North Wales which supplies Liverpool with tap water, is well-known to those who watch Springwatch on BBC television. The surrounding land is managed by the RSPB and in case any readers wonder where exactly the vole surveys of the late 1930s were done, I have drawn them on the map produced for visitors to the reserve. The habitat is though probably not suitable for Field Voles. At the time of the studies trees had been planted for forestry but the open nature of the ground remained vole friendly. That is probably not the case now but never having been to Lake Vrnwy I do not know.

The RSPB current map with the study areas from the 1930s marked in RED

     

After reading about vole cycles and the lack of any settled view on their cause I was left feeling that a long-term study should be done in a suitable habitat, applying all the knowledge of how to do such research that has accumulated over 80 years. While the same areas around Lake Vrnwy may not be suitable, why not repeat the studies elsewhere?

Dennis Chitty
from obituary by Charles J Krebs
for the
Royal Society of Canada

from Acta Theriologica 42, 1997

*The editor was Hugh Cary Gilson (1910-2000) a freshwater biologist who from 1946 to 1973 was Director of the Freshwater Biological Association.

†A good definition of maternal effects was provided by Mather & Jinks in 1970: Maternal effects arise where the mother makes a contribution to the phenotype of her progeny over and above that which results from the genes she contributes to the zygote. 

1.Charles Sutherland Elton FRS, 1900-1991

2.John Sherwood Perry, 1917-2010

3.Henry Neville "Mick" Southern, 1908-1986

4.John Rigarlsford Clarke, ca 1925-2010

5.John Guest Phillips FRS, 1933-1987

6.John William Sutton Pringle FRS, 1912-1982

7.William Peter Crowcroft, 1922-1996

8.Dennis Hubert Chitty, 1912-2010

9.Peter Brian Medawar OM FRS, 1915-1987

10.David Lambert Lack FRS, 1910-1973

Chitty D. 1952. Mortality among voles (Microtus agrestis) at Lake Vrynwy, Montgomeryshire in 1936-9. Philosophical Transactions of the Royal Society B 236, 505-552.

Chitty D. 1996. Do Lemmings Commit Suicide. New York: Oxford University Press.

Crowcroft P. 1991. Elton’s Ecologists. Chicago: University of Chicago Press.

How—and why—do tadpoles fill their lungs?

Those of us who have watched and kept tadpoles will have noticed that sometimes they come to the surface to take in air. A recent paper shows that very young and therefore very small tadpoles cannot break through the surface tension of the water in which they live. However, they still manage to take in air by a process the authors call ‘bubble-sucking’.

Even three days after hatching and only 3 mm long tadpoles have been found to fill their lungs. High-speed video showed what was happening. In five species of frog from North America and in the much-studied African Clawed Frog, Xenopus laevis the authors found: 

…mouth attachment to the water’s undersurface, the surface drawn into the mouth by suction, a bubble ‘pinched off’ within the mouth, then compressed and forced into the lungs. 

As tadpoles grow, they gain the size and strength to breach the surface of the water to take in air. However, larger tadpoles of one species studied (Grey Treefrog, Hyla versicolor) continued to use bubble-sucking exclusively while those of others used both methods until metamorphosis.

The authors recorded a similar of taking in air in salamander larvae which have external gills.

From Schwenk & Phillips 2020

It would be easy to assume that tadpoles take in air in order to extract the oxygen it contains. Tadpoles would normally be expected to respire through their gills and skin. With low concentrations of oxygen in the water, hot or fetid, for example, the selective advantage of being able to breathe air is obvious. However, the presence of air in the lungs is related to another function in these aquatic organisms—the control of buoyancy. I am surprised that the authors in their discursive account chose to concentrate on a presumed respiratory function when there has been a considerable amount published on air in the lungs in relation to the control of buoyancy. The authors themselves noted that in at least one of the species studied the lungs at 3 days after hatching are poorly vascularised and do not acquire a rich blood supply typical of a site of gaseous exchange until later in development. 

Tadpoles, by having the ability to fill their lungs with air using the newly discovered method of ‘bubble-sucking’ to overcome the surface tension of water, thus have the opportunity to use that air for the control of buoyancy and as a source of oxygen, depending on their stage of development and the degree of oxygenation of the water in which they live.

And I am still fascinated by tadpoles despite the strictures of my grandfather that I would never be able to make a living by studying them.

Schwenk K, Phillips JR. 2020. Circumventing surface tension: tadpoles suck bubbles to breathe air. Proceedings of the Royal Society B 287: 20192704. http://dx.doi.org/10.1098/rspb.2019.2704 

see also

Gee JH, Rondeau SL. 2012. Strategies used By tadpoles to optimize buoyancy in different habitats. Herpetologica 68, 3-13 doi.org/10.1655/HERPETOLOGICA-D-10-00023.1