Rovinj: The Sheffield Zoology Field Trip in 1964. Part Three. Reptiles and Amphibians

Algyroides nigropunctatus
from Hellmich

In writing about Sheffield Zoology’s first field course in Rovinj now in Croatia and then part of Yugoslavia at Easter 1964, my mind wandered into the difficulties we encountered in identifying the reptiles and amphibians from the surrounding countryside and town. With the wealth of information now available both in print and online it must be difficult to appreciate that nearly 60 years ago the only source on European species in English was a book by Walter Hellmich¹ published in 1962. I took that with me.

Some specimens were easy to identify from the limited number of illustrations and descriptions. But a juvenile snake (later identified as the Balkan Whip Snake) and what seemed to be one, but possibly two, species of lizard was more problematical. They ended up, and I cannot remember how, with a GP in Wolverhampton, Dr John V. Tranter² who was very active in amateur herpetological circles in the West Midlands. He got hold of a copy of the standard German checklist³ of the time by Robert Mertens and Heinz Wermuth as well as consulting Boulenger’s catalogues of specimens in the British Museum. He found all the unknowns, including those I suspected from the descriptions in Hellmich were the Dalmatian Wall Lizard. That species, originally Lacerta melissellensis⁴ but now Podarcis melissellensis, is now well-known to be polymorphic. In short there were two forms of this species around Rovinj, with one more common than the other. The least common bore a striking resemblance in terms of coloration to the Italian Wall Lizards seen and collected in the area but of lighter build and with smaller, less-pointed jaws.

We finally identified all the species (with current scientific names shown):

Bufo bufo. Common Toad

Bufotes viridis. Green Toad

Hyla arborea. Common Tree Frog

Lissotriton vulgaris. Smooth or Common Newt

Algyroides nigropunctatus. Dalmatian Algyroides, Keeled Lizard

Podarcis muralis. Common Wall Lizard

Podarcis siculus. Italian Wall Lizard

Podarcis melissellensis. Dalmatian Wall Lizard

Pseudopus apodus. Glass Lizard. Glass ‘Snake’, Scheltopusik

Hierophis gemonensis. Balkan Whip Snake

Podarcis sicula campestris
from Hellmich

In our meanderings through the countryside during the late afternoons until, on some days, dusk, we encountered almost nobody. On the edges of the town, the local human inhabitants were at first wary but after establishing that we were not Germans were friendly and helpful. Sons and daughters learning english at school were summoned to translate as best they could and their fathers and grandfathers became even friendlier when I told them that my father had not only been stationed on the island of Vis and had met Tito and his partisans but that he had been through Croatia in the back of an army lorry as far south as Pula in 1945. Eventually the conversation turned to reptiles and they explained to me that in late March only the small lizards and snakes appear from hibernation. In April-May, they said, we could have expected to see larger lizards and snakes as well.

As a matter of interest, I wondered recently what other reptiles are known to occur in the area around Rovinj. I looked at the distribution maps in the 2016 Field Guide⁵ and came up with the following list in addition to those shown above:

Salamandra salamandra. Fire Salamander

Triturus carnifex. Italian Crested Newt

Bombina variegata. Yellow-bellied Toad

Rana dalmatina. Agile Frog

Pelophylax kl. esculenta. Edible Frog

Pelophylax ribibundus. Marsh Frog

Testudo hermanni. Hermann’s Tortoise

Emys orbicularis. European Pond Terrapin

Tarentola mauritanica. Moorish Gecko

Hemidactylus turcicus. Turkish Gecko

Lacerta viridis, Eastern Green Lizard

Zootoca vivipara. Viviparous Lizard

Slow Worm. Anguis fragilis

Hierophis viridiflavus. Western Whip Snake

Elaphe quatuorlineata. Four-lined Snake

Zamensis longissimus. Aesculapian Snake

Coronella austriaca. Smooth Snake

Telescopus fallax. Cat Snake

Natrix natrix. Grass Snake

Natrix tessellata. Dice Snake

Malpolon insignitus. Eastern Montpelier Snake

Vipera ammodytes. Nose-horned Viper

There are a number of reports, mainly from amateur German and Austrian herpetologists, on field trips made to the same area. The nomenclature varies a little because there has been argument over whether, for example, it is the Eastern or Western Green Lizard (L.bilineata) that occurs there while the status of pool frogs, Pelophylax, remains problematical.

We have never been back to Rovinj. Looking at the area on Google Earth there seems to have been considerable expansion of the town. The countryside looks to have been tidied up and I wonder how many areas of scrub with large boulders inhabited by Algyroides have survived. I shall never forget walking along a country lane and hearing a noise which sounded like a huge flock of geese. Only as we got nearer and found no geese did we realise the sound was coming from the bushes and small trees surrounding a pond. The noise was being emitted by male tree frogs, gathered in the early spring waiting for females (a few were around the edges of the pond) to arrive.

European Tree Frog

Green Toad

Common Toad

The above photographs were taken with my Rolleiflex 4 x 4 on Agfacolor CT18 reversal film. Lighting was from a flashbulb. A more unsuitable camera for close-ups would be hard to imagine because of the nature of a twin-lens reflex. The camera was focused through the viewing lens and then raised by the distance between the viewing and taking lens to remove the effect of parallax. Animals could and did absent themselves from the scene while that shift was being made, resulting in a wasted frame.

1 Walter Hellmich (1906-1974) was Chief Keeper of the Zoological Collection of the State Museum in Munich. His book was originally published in German in 1956 (Die Lurche Und Kriechtiere Europas. Heidelberg: Carl Winter). The English version is: Hellmich W. 1962. Reptiles and Amphibians of Europe. (English Editor Alfred Leutscher). London: Blandford.

2 Died 2 November 2014, aged 79

3 Mertens R, Wermuth H. 1960. Die Amphibien und Reptilien Europas. Frankfurt: Kramer. Robert Mertens (1894-1975) and Heinz Wermuth (1918-2002) had revised an earlier checklist by Mertens and Lorenz Müller (1868-1953) (the latter was Hellmich’s mentor in Munich). There was at the time an inordinate fondness for describing subspecies, an enthusiasm I do not share.

4 Named for Melisello, now called Brusnik, an islet near Vis.

5 Speybroeck J, Beukema W, Bok B, Voort J van der, Velikov I. 2016. Field Guide to the Amphibians and Reptiles of Britain and Europe. London: Bloomsbury.

Peaker M, Peaker SJ. 1968. Spring herpetofauna of the Rovinj area (Istria, Yugoslavia). British Journal of Herpetology 4, 36‑37.

Lilge D, Wicker R. 1972. Bemerkungen zu den Eidechsen der Umgebung von Rovinj (lstrien). Salamandra 8, 128-136.

Edward Bles. Part 4. Cambridge: Olms and Paul Kammerer

At the end of April 1923, 12 Madingley Road had a house guest. Edward and Bertha Bles were entertaining Paul Kammerer who had been invited to give a talk to the Cambridge Natural History Society about his claims on the inheritance of acquired characteristics. Bles and Kammerer would have had much to talk about since both kept and bred amphibians, and three of Kammerer’s claims centred on such species, the Midwife Toad (Alytes obstetricans), the Fire Salamander (Salamandra salamandra) and, to a certain extent, the Olm (Proteus anguinus).

The lecture at Cambridge provided the opportunity for a verbal punch-up between the neo-Darwinists and the neo-Lamarckians. Discussion at the time was concerned with the possibility that the scientific world was being gulled by a plausible fraudster. Despite the efforts of some to resurrect Kammerer’s reputation, notably the mystic and over-taken-notice-of Arthur Koestler with his book, The Case of the Midwife Toad, informed opinion seems to have swayed towards the view that Kammerer’s studies were fraudulent since there are plausible explanations as to how he, possibly with the assistance of others, had contrived to present doctored evidence that favoured his Lamarckian hypothesis.

There is a letter from George Albert Boulenger mentioned in Koestler’s book stating that Bles had visited Kammerer in Vienna at some time around 1908, so their meeting, at which all parties would have spoken German given Kammerer’s limited conversational English, would have been an opportunity to catch up. It would have been interesting to know if Hans Gadow (1855-1928) was also present. He helped Kammerer by translating the discussion at the Cambridge lecture but was not impressed by his science. Gadow was another amphibian enthusiast, notably writing the classic volume in the Cambridge Natural History series, but also keeping and breeding them at his house Cleramendi (since renamed) on Hinton Way at Great Shelford. I get the impression that Bles and Gadow were close; they operated as a team as two of the local organsers of the 1898 zoological congress held in Cambridge.

Both Kammerer and Bles had kept Olms, the cave-dwelling blind salamander of south-eastern Europe. Kammerer claimed to have bred them in captivity, a claim now strongly disputed since his ‘findings’ bear no relation to what has been observed either before or since, i.e. that they are viviparous and breed every year or so. Both had found that when kept in the light, the normally white animals turn black. Bles got there first on that one since Hans Gadow in his book published in 1901 wrote:

Mr. Bles has succeeded in producing several totally black specimens, having kept them for several months in a white basin under ordinary conditions of light. No experiments have yet been made to find out if the black pigment deposited is lost again in darkness.

Kammerer also claimed that eyes became larger when they were kept under alternating red light and daylight. When the skin over the eyes was removed, a specimen with normal eyes was produced. An alternative explanation, that he might have obtained such a specimen from a natural population in this highly variable species, has been advanced. However, Kammerer does not appear to have claimed that Olms with eyes or which had turned black produce young with these characteristics, as some neo-Lamarckists seem to have imagined.

Embed from Getty Images

In a previous post (here) I have described how it was intended to repeat and extend Kammerer’s experiments with Olms at London Zoo in the 1930s under the direction of Ernest W. MacBride, arch-lamarckist, Kammerer’s vicar on earth and a powerful, dogmatic but totally misguided figure in British science during the early decades of the 20th century. He also, incidentally, assumed the role of ‘Master of Ceremonies’ at the Cambridge lecture where it was said, ‘old MacBride’s ridiculous ex-cathedra statements did not help’.

Edward Bles was reported as having found Kammerer ‘absolutely honest’. However, he was clearly not convinced by what he had been told or had seen. After all he did insist that the chair he funded at Cambridge should be named after Darwin.

Bles did not live long enough to see the sad end of Kammerer; he died suddenly on 3 May 1926. Three months later, on 7 August, a letter to Nature by Gladwyn Kingsley Noble (1894 –1940) appeared. It delivered a bombshell: the alleged black nuptial pad of the only specimen of Kammerer’s Midwife Toad that was said to have survived was Indian Ink. Kammerer shot himself and was found dead on an Austrian mountain path on 23 September.

Alphen JJM van, Arntzen JW. 2016. Paul Kammerer and the inheritance of acquired characteristics. Contributions to Zoology 85, 457-470.

Gadow H. 1901. Amphibia and Reptiles. The Cambridge Natural History Volume VIII. London: Macmillan

Koestler A. 1971. The Case of the Midwife Toad. London: Hutchinson.

Edward Bles. Part 3. Mr Budgett’s Frogs and an abortive expedition to Paraguay

John Samuel Budgett died, aged 31, on 19 January 1904 of blackwater fever and malaria. He became famous because of his four expeditions to Africa in search of eggs and developing young of the strange fish, Polypterus. There had been all sorts of theories about Polypterus: that it was the ‘missing link’ between fish and amphibia; that it might even been an amphibian. Thomas Henry Huxley had considered it closely related to the the lungfish and the coelacanths, other fish with lobed fins. Eventually Budgett succeeded but did not live to present or publish the results. On the day of his death he was due to give paper to the Zoological Society of London. Polypterus is an ‘early’ finned fish, nowhere near any possible line of descent from fish to amphibian.

Budgett was following the Cambridge tradition established in the 1870s and 80s of using embryology as a tool to unravel evolutionary relationships. An exponent of the Cambridge embryological approach was John Graham Kerr. As a new graduate seeking to work on the lungfish, Lepidosiren, Kerr took Budgett on a collecting expedition in 1896/97 to the Paraguayan Chaco in order to collect material. During their trip Budgett also collected amphibians and reptiles. He found two new species, one of which. Lepidobatrachus laevis, is known as Budgett’s frog.

Budgett collected eggs and tadpoles in Paraguay as well as in Africa during his searches for Polypterus. Before his death he had worked on the development of one species collected in the Chaco. However, he left a great deal of material in Cambridge. At the time of Budgett’s death Kerr had moved from Cambridge to Glasgow, taking Edward Bles with him. Bles started to work on the eggs and tadpoles collected by Budgett both in South America and in Africa. Bles’s words take up the story:

When this material was handed over to me I was much impressed by its interesting character and still further impressed by the novelty of the Engystomid [narrow-mouthed] embryos of Hemisus and, as the series of stages of the last two forms were not extensive, I determined to make an effort to obtain more material and obtained six months leave for a voyage to S. America. I spent almost the whole of the time available—May to August 1905—at San Bernardino on Lake Ipacaraÿ in Paraguay. Unfortunately the winter was most exceptionally cold and there were great floods over immense tracts in Brazil, Paraguay, and the Argentine Republic. Lake Ipacaraÿ had also flooded its shores and my main objects, to collect vertebrate embryological material, were completely defeated. The frogs did not breed during that winter in Paraguay, the only tadpoles found were late hibernating stages. 

The area he chose was where Kerr and Budgett had collected nearly ten years earlier.  The eggs and tadpoles Bles was hoping to collect is now known as Physalaemus biligonigerus, the Four-eyed Weeping Frog. To get to Paraguay he sailed with his wife from Liverpool on 30 March 1905 on the S.S. Oravia heading for Buenos Aires. After what must been an extremely disappointing few months they arrived back in U.K. on 5 August, disembarking at Southampton from the S.S. Danube. Bles had suffered the well-known syndrome of ‘you should have been here last week/month/year; we were falling over them’.

Physalaemus biligonigerus (Raúl Maneyro)
http://calphotos. berkeley.edu

The African species Budgett collected was Hemisus marmoratus, the Marbled Snout-burrower or Pig-nosed Frog or even Shovel-nosed Frog. Bles wrote up the description of the development of both species for a chapter in a memorial volume in honour of Budgett and his achievements compiled and edited by Kerr. Kerr himself completed the Polypterus story. Cambridge University Press published the book in 1907; it was reprinted in 2014.

Hemisus marmoratus (Ryanvanhuysteen)

John Samuel Budgett

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.

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 

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

Frogs of China. Alice Boring’s Life and Work. 3. Herklots and Hong Kong Amphibians

As I mentioned in Parts 1 and 2 of this series Geoffrey Herklots sent specimens of Hong Kong amphibians to Peking for Alice Boring to identify. In the first of those papers all of which were published in Hong Kong Naturalist she wrote that the material was collected under the supervision of Dr Herklots for a period of a little over one year, from December 1930 to January 1932…Herklots had arrived at the University of Hong Kong in 1928 to teach biology, just like Boring in Peking, to medical students. Further specimens were sent in 1933 and possibly later but of these only one had not been represented previously. The specimens, number unknown, were collected on Hong Kong Island, on Lantau as well as in Kowloon and the New Territories.

Alice Boring identified 16 species (a 17th Herklots realised had been collected elsewhere and I have omitted any reference to it). To date 24 species of amphibians have been recorded in Hong Kong. Of the ones recorded before 1930 the Herklots collection missed only one.

The following is a checklist of Hong Kong amphibians, using the current scientific name. The ones marked § are those identified by Boring.

§Hong Kong Newt Paramesotriton hongkongensis

Leaf-litter Toad Leptolalax laui. First recorded in Hong Kong 1979

§Short-legged Toad Megophrys brachykolos (from tadpole as M. boettgeri and an adult tentatively as M. longipes )

§Asian Common Toad Duttaphrynus melanostictus

Hong Kong Cascade Frog Amolops hongkongensis. First recorded in Hong Kong 1950

South China Cascade Frog Amolops ricketti. First recorded in Hong Kong 2004

§Paddy Frog Fejervarya limnocharis

§Chinese Bullfrog Hoplobatrachus rugulosus

§Günther’s Frog Sylvirana (Hylarana) guentheri

Brown Wood Frog Hylarana latouchii. First recorded in Hong Kong 1984

§Three-striped Grass Frog Hylarana macrodactyla

§Two-striped Grass Frog Hylarana taipehensis

Big-headed Frog Limnonectes fujianensis (not recorded in Hong Kong between 1917 and 1987)

§Rough-skinned Floating Frog Occidozyga lima

§Green Cascade Frog Odorrana chloronata

§Lesser Spiny Frog Quasipaa exilispinosa (as Q. spinosa). Identified as species in 1975 (see below)

Giant Spiny Frog Quasipaa spinosa. Adults first discovered in Hong Kong 1978 (see below)

Romer’s Tree Frog Liuixalus romeri. Discovered in Hong Kong 1952

§Brown Tree Frog Polypedates megacephalus

§Spotted Narrow-mouthed Frog Kalophrynus interlineatus

§Asiatic Painted Frog Kaloula pulchra

Butler’s Pigmy Frog Microhyla butleri. First recorded in Hong Kong 1964

§Ornate Pigmy Frog Microhyla fissipes

§Marbled Pigmy Frog Microhyla pulchra

G.A.C. Herklots

As I read Boring’s papers I became intrigued about the two species of Quasipaa, exilispinosa and spinosa, now known to occur in hill and mountain streams. One, Q. spinosa is much larger than the other, reaching 14 cm—the largest anuran in Hong Kong. Although the drawing used to illustrate Boring’s paper is clearly of Q. exilispinosa (the webbing of the hind limbs does not reach the tip of the toes whereas in Q. spinosa it does) she wrote: ‘My material from Hong Kong includes two very large specimens and 7 medium-sized ones…’ Unfortunately, she provided no quantitative information but there remains the possibility that the collection sent by Herklots did contain the two species of spiny stream frogs rather than just the one.

This collaborative effort between Alice Boring and Geoffrey Herklots was the first organised survey of the amphibians of Hong Kong. It provided the basis on which others have built, starting, of course, with John Romer who began his activities soon after his arrival in the late 1940s.

I do not know if Boring and Herklots ever met. There was one opportunity in Hong Kong in 1937 when Boring, caught away from Yenching during the Japanese advance, made her way back to the university by first travelling south.

Paddy Frog (Fejervarya limnocharis)

Boring AM. 1934. The amphibia of Hong Kong Part I. Hong Kong Naturalist 5, 8-22

Boring AM. 1934. The amphibia of Hong Kong Part II. Hong Kong Naturalist 5, 95-107

Boring AM. 1936. The amphibia of Hong Kong Part III. Hong Kong Naturalist 7, 11-14

Karsen SJ, Lau M W-N, Bogadek A. 1998. Hong Kong Amphibians and Reptiles. Second Edition. Hong Kong: Provisional Urban Council