The Marsupial Frog and a Film from the 50s

The Film

When writing recently about ‘Amo’ (Emmanuel Ciprian Amoroso FRS, 1901-1982) and his interest in amphibians I remembered that that he had been involved in making a film about the Marsupial Frog, Gastrotheca sp, which he had kept and studied at the Royal Veterinary College in the 1950s. Amo’s life’s work was studying viviparity, particularly the mammalian placenta. The question was to what extent the mother provides oxygen and nutrients to the young of other vertebrates that are born alive or may, as in amphibians be stored in the body until they are released as tadpoles or young frogs. He was interested in this species because the eggs after fertilization are manoeuvred by the male into the mouth, just above the cloaca, of a backward-facing pouch on the back of the female. The eggs hatch there and the tadpoles grow are released into water at a stage shortly before development of the hind legs.

Amo was very proud of the film. Although the phenomenon of storing eggs in the pouch in these South American frogs was well documented, it is believed this was the first time the whole process had been observed and filmed. I then wondered if the film still existed and where it had been shown.

The first clue was the list of publications in Roger Short’s biographical memoir on Amo. There it is described as ‘1957 Reproductive phenomena in Gastrotheca marsupiata. R. Soc. Conversazione (23 May)’. Notes and Records of the Royal Society (12, 154-159, 1957) provides more information:

The second film was shown by Professor E.C. Amoroso, F.R.S., and Miss J.H Austin, of the Royal Veterinary College, and Dr. J.F.D. Frazer of Charing Cross Hospital, and was concerned with the reproduction methods of the frog, Gastrotheca marsupiatum, which is partially independent of water for its reproductive processes.

I then found that the film had been shown earlier, at a meeting of the Physiological Society at the Royal Veterinary College on 14-15 December 1956 (Journal of Physiology 135, 38P, 1957). There was no other information other than the title and ‘authors’ since the presenters could choose to have their contribution recorded ‘by title only’. The authors were shown as EC Amoroso, J Austin, A Goffin and E Langford. From the acknowledgements I have found that A.R. Goffin was a technician in Amo’s department of Physiology (he is thanked for taking photographs). Miss J.H. Austin in 1960-61 was then on the staff of the department of anatomy, possibly as a lecturer, at the RVC where she is listed in Scientific Research in British Universities and working on ‘development of gastrotheca’. She was not in the 1962-63 volume and I can find no further information on her or on E Langford.

Eventually I found that the film still exists. It is in the collection of the British Film Institute under the title 'Natural history of the large South American pouched tree frog Gastrotheca [originally listed as Gastortheca] marsupiatum'. BFI Identifier 21716. The entry in the catalogue indicates  the original was a 16 mm silent film of a surprisingly long 1500 feet, i.e. 42 minute running time. It is dated as 1955 with a ‘release date’ of 1954 which is unlikely. There is no indication in the BFI catalogue of who made the film or where it was obtained from.

Given the costs of licensing from the BFI I cannot see it ever being digitised or being made available for viewing.

There are lots of videos of Gastrotheca frogs on YouTube but I have not found one that shows the life cycle. In that important respect it seems that Amo’s film is so far unique. Beware though that in searching for ‘marsupial frog’ the best video is one from a BBC series which shows an Australian species, Assa darlingtoni, that has ‘hip pickets’ for its eggs, not a dorsal sac, and is unrelated to Gastrotheca species from South America.

A Publication

In 1957 Amo’s friend and erstwhile collaborator on reproduction and lactation in the Grey Seal (of which stories of their adventures were often related), Leo Harrison Matthews FRS (1901-1986) then Scientific Director at the Zoological Society of London, published a paper in Bulletin de la Société de France entitled, ‘Viviparity in Gastrotheca (Amphibia, Anura) and some considerations on the evolution of viviparity’. I have not read the paper (it falls into that category of too young to be in online archives and too old to be digital) but it clearly covered the same ground and probably the same frogs as the film. It is the only written record covering the breeding of these frogs in London around 1955-56 and has been referred to in later papers in relation to the identity of the frogs (see below).

Amo referred to his work on Gastrotheca in several of his reviews and conference papers but not in a full paper. In 1959 a photograph appeared in the published version of a talk he had given at a Josiah Macy Jr symposium on gestation in Princeton in 1958—again a paper I have been unable to find online. That was reproduced—and is shown below—in another paper, ‘The evolution of viviparity’, published in Proceedings of the Royal Society of Medicine in 1968.

Amo argued that because the eggs of Gastrotheca contain plenty of yolk, the developing young receive oxygen but little if any additional food from the parent. That may be the case in the species he studied but in another, Gastrotheca excubitor, which retains the young throughout the tadpole stage and in which froglets emerge from the pouch, recent evidence suggests the possible transfer of nutrients from the mother to the young through the wall of the pouch. Definitive evidence, though, is still lacking.

Origin of the marsupial frogs in London

Where did Amo get his frogs? Was it via Deryk Frazer who appeared as presenting the film at the Royal Society along with Amo and Austin? A clue exists in an article written by Bob Bustard for The Aquarist in 1958; he wrote:

…An example of this is Gastrotheca marsupiatum, appropriately called the pouched tree frog. I imported this frog into Britain for the first time in 1955, and it has become remarkably popular among vivarium keepers already. This is possibly because it does so well at about 65°F and will breed readily in a small indoor vivarium.

My bet is that the frogs at the Royal Veterinary College came directly or indirectly from Bob Bustard.

A paper also appeared in British Journal of Herpetology describing the breeding in captivity of ‘Gastrotheca marsupiatum’ in 1957 by a J. Walker. I have not seen this paper but my guess it describes animals obtained from Bob Bustard also.

Marsupial frogs were kept in UK throughout the 1980s and early 1990s at least. I do not know if they were newly imported or had been bred in captivity, or indeed were descendants of those imported by Bob Bustard in 1955. Gillett records captive-bred individuals for sale around 1957 and I knew of somebody with a pair in the early 1990s

Which species of frog?

The frogs kept and bred in Britain and in continental Europe in the 1950s and later were all called Gastrotheca marsupiatum or Gastrotheca marsupiata. Before moving on it is worth noting that the currently accepted name is G. marsupiata was that coined by Duméril and Bibron in 1841. The same species was called Nototrema marsupiatum by Günther in 1859. G. marsupiatum appears to have been mistakenly used as Gastrotheca came to replace Nototrema; there may also have been a little discussion over the gender of the specific name matching that of the genus.

But that is by the by. During the 1970s doubt was thrown on the identity of the frogs studied in the 1950s and beyond as G. marsupiata, notably by Eugenia M del Pino in 1975 and by William Duellman and Scott Maness in 1980. The latter listed a number of papers on the reproductive habits of, supposedly, G. marsupiata. That included the paper by Harrison Matthews and, therefore, by implication those in Amo’s film, although by then awareness of the existence of the film seems to have been lost. ‘All those works in which the origin of the specimens was given cite Quito, Ecuador’, Duellman and Scott wrote, continuing, ‘G. marsupiata does not occur north of Central Peru; the Ecuadorian frogs formerly associated with that species are G. riobambae’. As a result of this statement, the animals in captivity became to be referred to as G. riobambae. That view still obtains: captive-bred animals in the USA, Britain and continental Europe are listed as Gastrotheca riobambae—the Andean Marsupial Frog.

What I do not know is where the frogs Amo used for his film were originally imported from and if Duellman was correct in assuming that the frogs in captivity around and after that time were G. riobambae rather than G. marsupiata.

This is the first photograph of a marsupial frog I remember seeing. It is from Doris Cochran's Living Amphibians of the World, published in 1961 by Hamish Hamilton.
The photographer was the American, John H. Tashjian. Also in that volume were black-and-white photographs by Wilhelm Hoppe. All are captioned G. marsupiata. Are the photographs of G. marsupiata or G. riobambae?

This discussion serves to illustrate the value of ‘voucher specimens’ in research and captive-breeding projects. The same consideration applies to photographs since it is very difficult to know whether the animals has been correctly identified, especially those in captivity. With preserved specimens there would be no doubt about which species was being studied or bred. Does anybody have any preserved specimens from these early days of breeding marsupial frogs?

I will return to marsupial frogs in a future article, because their reproductive biology is so fascinating and because their storage of eggs and tadpoles presents physiological challenges that require further study, not the least of which is how the female’s own young avoid the fate of being rejected as non-self while being held in intimate contact with the mother’s body, a biological problem that haunted Amo and one which drove his interest not only in mammals but in reptiles, amphibians and fish.

I found this photograph of the meeting at which Amo (2nd right, front row) talked about marsupial frogs.
It is from the website on placentation by the late Kurt Benirschke (1924-2018)

For those seeking further information:

Amoroso EC. 1968. The evolution of viviparity. Proceedings of the Royal Society of Medicine 61, 1188-1200.

Bustard HR. 1958. Tree frogs. Aquarist and Pondkeeper 23 (4, July 1958), 81-82.

Duellman WE, Maness SJ. 1980. The reproductive behavior of some hylid marsupial frogs. Journal of Herpetology 14, 213-222.

Gillett L. 1995. The good old/bad old days. A survey of reptile and amphibian species traded during the period 1948-1957. British Herpetological Society Bulletin 1995 (52), 26-29.

Kirk BR. 1985. Observations on the breeding of the marsupial frog, Gastrotheca marsupiata. British Herpetological Society Bulletin 1985 (14), 22-24.

Matthews LH. 1957. Viviparity in Gastrotheca (Amphibia, Anura) and some considerations on the evolution of viviparity. Bulletin de la Société de France 82, 317-320.

Pino EM del, Galarza ML, Albuja CM de, Humphries AA. 1975. The maternal pouch and development in the marsupial frog Gastrotheca riobambae (Fowler). Biological Bulletin 149, 480-491.

Warne RW, Catenazzi A. 2016 Pouch brooding marsupial frogs transfer nutrients to developing embryos. Biology Letters 12: 20160673. http://dx.doi.org/10.1098/rsbl.2016.0673 

R Maxwell Savage: The Forgotten Doyen of British Ecological Herpetology Part 6: The Physics and Chemistry of Frog Spawn

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I am ending this series of articles on Maxwell Savage by discussing one small part of his research on the life of the Common Frog, Rana temporaria, in Britain: frog spawn.

Common Frogs lay spawn in clumps, not as single strands of eggs like the Common Toad, Bufo bufo. Savage realised that because the swollen jelly surrounding the egg is 99% water, the mass of spawn acts as a heat store for the developing embryos within. Unlike water in the pond, the water in the jelly is held and thus constitutes ‘a relatively enormous mass of solidified water’. Therefore, in sunlight the mass of spawn warms up. At night, because the warmed ‘solidified water’ cannot go anywhere, the only way for heat to be lost is by conduction and since water is a very poor conductor the heat is retained. Savage did experiments at home and in the field. He showed that in 63 cases out of 73, the spawn was warmer than the surrounding water. The  average difference 0.63°C, not a big difference Savage noted, but one which could have given an important advantage to repopulation after the last Ice Age.

He also investigated the structure of the mass of spawn itself. It is not an amorphous mass but structured in a way ‘which may be likened to a bunch of grapes glued together only where they touch’. Therefore, water circulates freely within the mass of spawn and oxygen for respiration only has to pass across the jelly the distance of one half of the diameter of the individual egg. He demonstrated this structure by dropping Indian ink on a freely floating mass; the ink passed through in a very short time.

The corollary of this demonstration of the structure of the spawn mass is that if a mass of frog spawn is laid or later held in water of insufficient depth the inner channels are blocked by collapse of the mass.

Savage also became involved in studying the events that lead to the ovum being surrounded by coats of jelly on its passage through the oviduct, which swell on contact with pond water after fertilization. I will not dwell on the aspect he examined—the inner gel that surrounds the ovum—but it is of historical interest and possible physiological importance. Savage wrote:

By a coincidence, Dr. Burgess Barnett and I shared a common interest in two unrelated scientific fields—the study of amphibia and of blood-clotting. In May 1939, Dr. Barnett, who had just left the Zoological Society of London, where he had been the Curator of Reptiles, for a similar post at Rangoon, wrote to say that he had ‘‘stumbled upon* a curious property of the frog’s egg. The jelly contained a clotting factor which he likened to the prothrombin of blood. He invited me to collaborate m its investigation, and when I accepted he sent me the only notes that he had. They consisted of some tests on normal and on haemophilic blood. In 1939, the subject of blood-coagulation, although it already had a large literature, had not grown to the enormous extent that it has now assumed, and in the light of more recent knowledge, it is clear that the factor he had discovered was not prothrombin, but a variety of thromboplastin [thrombokinase]. Thromboplastins are rather widely distributed in nature, sometimes occurring in unexpected places, and if this had been the only point, there would have been only a mild interest in the fact. From Dr. Barnett’s letters it seems clear that he had not any idea of the possible function of the factor, and very tentatively he suggested that it might be protective…Before we reached the point of actually collabo­rating, Dr. Barnett died. There the matter remained, until in planning this chapter I realized the probable function of the factor and the part it may play in the ecology of the frog and very likely in the lives of other species as well.

Savage’s experimental evidence suggested that some form of clotting process was involved in the solidification of the inner layer of jelly.  I have found no particularly relevant further research but for several descriptions of various numbers of layers of jelly in different species and some of their molecular components. I will leave the last word on this topic to Savage:

This rather complicated story of the formation of the jelly envelope may, then, be summarized as follows. The vitelli [ova] pass into the oviduct. There they form the nuclei round which collects the insoluble product of a clotting system, in which a factor resembling the thromboplastin of blood contributes to a transformation that has something in common with the similar transformation that occurs when blood clots. The protein is not the same, and the rest of the process probably differs considerably. This protein layer is fairly concentrated. When it has formed, the eggs pass into the ovisac, where they become distributed in a fairly concentrated solution of a different protein. When they are ejected by the frog, the mass passes into water, salt is removed and the protein precipitates, forming the second and outer layer of jelly. Both layers now imbibe water, and in twenty-four hours or so achieve maximum size. In this process, the outer layer is stretched by the swelling of the inner layer, and gives way except at the points of contact of the spheres, where there is no stress. The final result is that a mass of adherent spheres is formed, with channels in between. The final percentage of structural protein in a blood-clot and in frog-jelly is about the same, but the clot and the jelly approach this concentration from opposite directions: the jelly swells, but the blood-clot is formed full size at once and, indeed, tends to shrink. 

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This is the last in my series on Maxwell Savage, the forgotten man of herpetology in Britain. After searching for information on Savage and producing a short biography Trevor Beebee wrote:

“Ecology and Life History of the Common Frog” is a seminal achievement, bringing all his earlier work together in one book as a very readable monograph. The research is all the more remarkable because it was carried out in his own time, with no external funding – just his own energy and enthusiasm. Among other things, the book also hints at how dramatically frogs declined in the countryside between the 1930s/1940s, when he found ponds with thousands of spawn clumps, and the late 1950s, when only a few of his old study ponds had any spawn at all.

I place Savage at the pinnacle of the small band of people in Britain who have investigated the lives of amphibians and reptiles. He asked simple, important questions about the life of the Common Frog at all stages of his life history which he attempted to answer by any means necessary.  Ronald Henry Maxwell Savage cast light. Every time we see a frog we should remember him, his research, and encourage others to take up the challenge of testing his hypotheses and thereby illuminate still further the life of amphibians and how they work.

R Maxwell Savage: The Forgotten Doyen of British Ecological Herpetology Part 5: Algae and Breeding in Xenopus

Maxwell Savage argued that not only does the smell of algae attract Common Frogs to ponds but that a chemical from algae actually initiates spawning. However, the Common Frog is not a convenient species in the wild or in captivity to test that hypothesis and so in the 1960s he shifted his entire effort to Xenopus laevis which he kept at home in banks of linked aquarium tanks.

Xenopus laevis
By Brian Gatwicke on Flickr

There is, of course, no reason to suppose that the demonstration of an effect of algae on the highly aquatic Xenopus would indicate that a similar mechanism was at play in Rana temporaria only that if it happened in one species the possibility that it could apply to another would have to be entertained. Breeding in Xenopus is very different from the annual spawning of Rana temporaria. In warmer parts of Africa, spawn may be produced all-year round, or during the whole breeding season in South Africa.

Savage published two papers on Xenopus, his last papers on any subject. The first, a letter to Nature, was in 1965; the second, in Proceedings of the Zoological Society of London, in 1971.  Sadly, it appears that both were poorly refereed and edited since they both suffer from the defects  noted by reviewers of his 1961 book: immense detail on some matters; scant detail on others. This is a great pity because it makes drawing conclusions difficult for those reading his papers 50 years later. I suspect the problem is that, as good a scientist as Savage was, he never went through that scientific writing apprenticeship experienced by those employed in research institutes and universities. That may be one of the reasons his work has been set aside or ignored by later workers.

His experimental set up at home, first in Hadley Wood and then, after he retired, at Welwyn, was designed to hold pairs of frogs in different compartments through which water was recirculated. Some compartments were lit; others were kept dark. He noted that hornwort, Ceratophyllum, and filamentous algae grew in the lighted compartments but there was never a bloom of free-living algae. There were a number of complications in the set-ups and management the two houses which make interpretation of the results more difficult. For example, water was partially changed for fresh well water at the same time as pairs were moved to different compartments; the temperature regime at the two houses was different; pairs spawned sometimes without apparent stimulus. Some compartments suffered low dissolved oxygen concentrations and low numbers of spawning occasions. This reliance on dissolved oxygen in the water was explained by the fact that the male in amplexus is kept with its head under the water and needs to rely on oxygen uptake through the skin. With insufficient oxygen in the water the male frog either drowns or breaks his grip and breathe air. Not surprisingly most males, but not all, chose to live and fertilise spawn another day.

Savage went to great lengths to ensure the randomisation of pairs of animals in the various compartments of his tanks, with each pair being reallocated a different compartment each week or, later, 10 days, according to random number tables. He also initially relied on the presence of spawn to test whether and external substance had worked or not. Then he realised that changes in behaviour may occur if not spawning itself, particularly in males; wach evening he scored each male ranging from 0 (no activity) up to full amplexus (4).

In his Nature paper there appears to have been no hornwort or other ‘higher’ plant present initially. He then compared the effect of adding ‘weed from natural ponds’ to compartments upstream of the ones in containing the animals. The nature of the ‘weed’ was undefined. One half of each bank of compartments was brightly illuminated; the other was covered with a dark cloth. Savage thus had four treatments: no weed, dark; no weed, light; +weed, dark; +weed, light. Spawning’ was attributed to weed when it occurred within four days from the addition’. These were his results:

Savage interpreted these findings as showing that a substance produced by algae, part of the ‘weed’ from natural ponds stimulated spawning. Assuming that the ‘weed’ was some ‘higher’ water plant like hornwort and not just a mass of filamentous algae, he does not appear to have considered the ‘higher’ plant could have been the source of a stimulatory material. His next step was to add algal monocultures to see if they induced spawning. He used a variety of cultures and treatments of the culture including, for example, two species of Chlamydomonas, an unidentified species found in ponds in which frogs spawn, culture medium sterilized three weeks earlier to kill the algae.

Savage bulked all these treatments which in the table of results he called ‘weed’ and compared them with untreated ‘no weed’ frogs. Observations were made each day for a total of 157 days on six pairs of frogs (randomised as described above). He counted each day as a trial, giving a grand total of 943 (157 x 6) trials. For ‘weed’ (i.e algal culture added) days he multiplied the number of additions of ‘weed’ by 6 and by 4, the number of days after treatment a positive score could be recorded. That product came to 312, and the number of trials on ‘no-weed’ days was, by difference, 630. Days when spawn was observed were 18 for ‘weed’ and 10 for ‘no-weed’ indicating an approximately 4-fold effect of adding algal cultures on the incidence of spawning. From the constructed 2 x 2 table, he obtained a P value of <0.005,

In Savage’s 1971 paper a similar regime was followed but with 8 pairs of animals and 10-day periods between water changes and pairs being allocated to a different compartment. Again he bulked results from all the preparations of algae, filtrates, concentrates and pure chemical (see below) and compared them with frogs not exposed to the additions on day 5 of the 10-day period. The incidence of spawning in the treated frogs was approximately 2.5-fold higher (eggs produced on 76 of 2120 days with the addition of algal preparations vs eggs on 47 of 3192 days)

The calculated effect was likely to have been be an underestimate, as Savage explained:

…(1) The same female does not spawn every night of the stimulus period. Often, other females spawn when she does not. Although, clearly, there was activity all this time, the total number of nights when some of the females do not spawn contribute to the cell “stimulus-no eggs”. (2) There was no way of knowing whether the substance in any particular experiment was active. Some prepara­tions were probably not active, and contributed to the same cell as in (1).(3) The dissolved oxygen effect [see above]…had not been discovered in this period, although it was known that sections 1 and 2 were relatively ineffective. This again distorts the Table.

He went on:

The results are unquestionably significant, but not sharp, in the sense that the additions of substances did not always produce spawning in every female every night.

After getting these results he went on to make an attempt at finding out what the chemical was that was stimulating spawning. For all of his work on Xenopus he had turned himself into an algologist, culturing various species for long periods. He also used his chemical knowledge to deduce from the various extraction, dfistillation and analytical procedures the possible nature and identity of the molecule(s) involved.

He knew, for example, that some freshwater algae produce steroids as well as metabolites which they release into the water. One of the latter is glycollic acid (or glycolic acid) which is secreted during photosynthesis and then taken up again at night by the same or other algae. He filtered an algal culture, acidified it to pH 5 and distilled the solution under reduced pressure. Both filtrate and the residue were active in stimulating spawning. After testing with various reagents he realised he had isolated glycollic acid. Therefore, he tested pure glycollic acid (it is used in cosmetic preparations as a skin exfoliant) to see if, like the algae and extracts, it would stimulate spawning. He used spawning and behaviour of the males as indices of activity. His results showed clearly that glycollic acid in the water stimulated reproductive behaviour and, when the dose was high enough, spawning. The incidence of eggs being produced was 5-fold higher compared with untreated control animals.

A eureka moment one might have thought. However, Savage realised argued that glycollic acid could not be his putative substance from algae that attracted frogs to the breeding pond. It is non-volatile and odourless. He thought it far more likely that glycollic acid is an intermediate in the synthesis of the actual stimulating chemical by the plants. That, he wrote, would explain why glycollic acid was far more effective when given in the spring, when plant growth is high, rather than in the autumn.

Scendesmus, one of the algae
cultured by Savage

In the summary of his 1971 paper Savage described which algal preparations were active when introduced into the aquarium water, although he presented no statistical data on this point:

(a) unialgal cultures of Chlamydomonas pulsatilla and of a species of Scenedesmus; (b) filtrates from cultures of Scenedesmus; (c) isopropanol extracts of dried cells of Scenedes­mus; (d) glycollic acid; (e) a fatty or waxy material isolated from Scenedesmus filtrates, or from aquarium water to which a culture has been added, by means of reversed phase column chromatography. 

The best material is an extract from the media, and this has been effective at one part in two million of aquarium water. It is still impure, and the true activity may be greater 

by a factor of 100. 

But Savage had not quite finished. I suspect he was still doing more work while the paper was in preparation for publication since he added a ‘Biochemical Appendix’. In it he provided crude chemical evidence that the algal extracts contain one or more steroid hormones. He also knew that addition of progesterone to the water, like a shot of gonadotrophins used to breed Xenopus for pregnancy tests, was followed by a single spawning and then a cessation of activity. That cessation was unlike natural spawning or that seen after the addition of algal extracts. He proposed a hypothesis to explain the puzzling effect of water changes on spawning activity:

…Let it be supposed that two substances are involved, one of which is not a hormone but a precursor, and is of fairly high stability in the aquaria, and the other, unstable, is a hormone derived from it by microbiological processes in the aquarium water. Microbiological processes are of great importance in steroid chemistry, sometimes providing the only route to a desired structure. The concentration of hormone in the water will then depend on the resultant of the two rates of formation and destruc­tion of the hormone, and could be greatly influenced by the profound modification of the micro­ biological environment produced by WC/R [water change/re-randomisation]. A very small concentration of hormone could be effective in frogs living continuously in the water. 

The first part of the hypothesis has been confirmed by adding an extract to the aquaria, waiting three days, running off 10 1. of the water and recovering the usual ketone. 

The second part has been confirmed, without any intention, by an experiment in the isolation of such a substance from a natural pond at the time when R. temporaria was spawning there, and by this means to establish a connection between the two species in their sexual activity. At the same time, the opportunity of fractionating the extract was taken, almost all the extracts having been used on the frogs in a crude state.

10 l of the water from the pond was processed in the usual way. The crude extract (165 mg) was dissolved in cyclohexane (10 ml.) and extracted with five lots, each of 10 ml. of N/1.NaOH. The alkaline extract was acidified, and extracted with five lots, each of 10 ml. of 1.1.1 trichlorethane, and the product (10 mg) subjected to Girard fractionation. The ketone fraction (0.6 mg) (clearly impure) and the non-ketones (3-6 mg) were added to line A and B respectively, on 24 March…The final activity was very similar in both—a male score totalling 23 in line A and 26 in line B, with four lots of eggs in line A and three in line B. The timing was quite different. All the activity in line B was before WC/R, but all the eggs, and more than half the male activity in line A was after WC/R. The correspondence with the hypothesis seems good. 

Fast forward to 2021 and we know that algae are indeed a rich source of biologically active phyto-oestrogens.

It would seem that Savage was searching for a single chemical constituent secreted by algae to explain the attraction of Common Frogs to ponds and the timing of actual spawning in both the Common Frog and in Xenopus. That seems an unnecessary assumption and it may be better to think in terms of several putative substances released by algae that could act in different ways and at different times on the animals.

I have described Maxwell Savage’s work at some length because it shows how he built up the case of a causal link, not just an association, between the presence of green algae and breeding in both the Common Frog and Xenopus. These experiments on Xenopus (with that final link between the two species in which he tested extracts taken from pond water in which Common Frogs were spawning) were Savage’s last published word from his 40-year study. However, before moving to the final section of this article, I think it is worth pointing out that Savage had found an earlier report of algae having a possible stimulating effect on Xenopus. Edward Bles was the first person to breed Xenopus under controlled conditions and Savage wrote:

Some observations by Bles seem to have been overlooked. His paper seems to show that he sometimes added a pure culture of Chlamydomonas to his aquaria to induce spawning, and that he suspected that some event in the microflora influenced his animals.

Although the 1971 is the last I have found, Trevor Beebee noted that Savage was ‘still experimenting with Xenopus in 1974. probably in the same garage laboratory where one of his grandsons recalled sleeping on a camp bed “under the whir of the aquariums where my dreams were soaked in croaks and plops”’. 

Getting to the end of revisiting Maxwell Savage’s research on frogs and algae—but not quite at the end of the series—I remain amazed that with so many ways in which his observations, inferences and experiments could be followed up by direct, simple experiments nobody has actually done so. There are experiments crying out to be done. For example, would Common Frogs be attracted to a pondless area of ground in by the smell of chemicals now known to be responsible for the odour of various algae? Does glycolic acid stimulate Xenopus to spawn directly, rather than as argued by Savage, being involved in the synthesis of substances that do?

Neither the seemingly endless observational studies nor or the current fixation with genomics will provide the answers. But simple experimental biology can. We owe it to Maxwell Savage to just get on with it, and settle once and for all whether there is a causal link between algae and reproduction in any species of amphibian.

Beebee TJC. 2010. Ronald Maxwell Savage, 1900-1985: a tribute. Herpetological Journal 20, 115-116.

Savage RM. 1965. External stimulus of the natural spawning of Xenopus laevis. Nature 205, 618-619.

Savage RM. 1971. The natural stimulus for spawning in Xenopus laevis (Amphibia). Proceedings of the Zoological Society of London 165, 245-260.

Sychrová E, Štěpánková T, Nováková K, Bláha L, Giesy JP, Hilscherová K. 2012. Estrogenic activity in extracts and exudates of cyanobacteria and green algae. Environment International 39, 134-140.

And Chlamydomonas, another algal species cultured by Maxwell Savage:

R Maxwell Savage: The Forgotten Doyen of British Ecological Herpetology Part 4: The Smell of Algae

Maxwell 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.

His hypothesis was based on his earlier observations on the food, or at least the gut contents, of tadpoles of which algae formed a large part; no point in spawning in a pond with no algae. In addition he found that frogs spawned in ponds with higher phosphate and potassium concentrations, in other words water ideal for the growth of plants. He suggested that in summer ‘higher’ plants grow rapidly and deplete the water of minerals. Runoff from rain in the winter then carries minerals, particularly phosphate, into the ponds which then leads, with increasing length and intensity of daylight, to an algal bloom and it is the smell of the algae that frogs take as their cue to migrate to the source of the odour. In essence he provided an explanation for the effects of amounts of rainfall in the months before spawning on the timing and direction of migration as well as the choice of pond.

Cartoon illustrating Maxwell Savage's hypothesis 

Savage realised that a problem arose with frogs moving to ponds against the direction of the wind. He suggested that various physical phenomena involving different movement of air at ground level, in ditches which frogs often use to reach ponds, and eddying could overcome the objection.

Savage further argued that it is possible to dispense with some substances in or produced by ponds as possible attractants. The first is water itself or the direct effect of rainfall since many frogs hibernate in ponds or very damp surroundings from which they migrate to a breeding pond. Then there were carbon dioxide (ubiquitous), ammonia (frogs would be ‘drawn to manure heaps’) and hydrogen sulphide (probably not released into the air), methane (again ponds would not be the only source). Instead he firmly came down on the side of volatile organic compounds produced by algae:

…It is, however, not the higher plants that do this [impart the characteristic of pond water], but the algae. There is much information on this matter, for it is of economic importance. If certain species of algae grow in drinking-water reservoirs to too large an extent, the consumers complain that the water tastes or smells. The odours are not always unpleasant, but people do not like water that has a strong smell or taste, whatever it is. The odours are due to essential oils elaborated by the algae, and the smells are so characteristic that a skilled person can detect and identify the species of alga sometimes before it can be located under the microscope. I once detected a smell from a pond (Large Totteridge) many yards from the bank, and suspected from the textbook description that it was due to Synura livella[*]. Micro­scopic examination showed that this species was abundant in the water 

     The fit of this hypothesis with most of the facts in the field is very good. The smells are found in ponds—nowhere else in the whole countryside. Any particular smell is probably only found in a few ponds for there are so many species of algae that, in a limited area, there are hardly any two ponds with the same flora. Ponds tend to have the same species in successive years, but this is not invariably so…

The observational and statistical associations that Savage unearthed make a compelling case for the central role of aquatic algae; they tie everything together. As good as Savage was in observing and drawing evidence from lots of different fields into a plausible hypothesis, the fact remains that there have been no experimental tests of what remains a fascinating possibility at least and a high probability at best.

There are two points to stress at this stage. The first is that Savage’s hypothesis concerns one species, the Common Frog, Rana temporaria. Various species of amphibian are now known to use a variety of mechanisms for navigation during migration. The evidence that frogs head for the pond in which they grew as tadpoles as their breeding pond (‘homing’) now seems to be strong and it is here that evidence suggests that Savage’s algal hypothesis cannot be the whole story. I have seen frogs accumulating on the earth of three filled-in ponds at the normal time of breeding; in two cases spawn was laid with no hope of its survival. (A similar phenomenon has been observed in toads.) Were these frogs that had not strayed far and using a local memory map to return home? Would frogs from further away not have been drawn to the bare earth of a filled-in pond?

Savage was clearly disappointed by the reception given to his hypothesis while realising the difficulties in taking things further, as demonstrated by the following extract:

It would be quite wrong to conclude this chapter leaving the reader with the impression that the algal hypothesis has been universally accepted. In fact, it is probably true to say that the general attitude has been one of polite incredulity…

And:

Frogs live their aquatic life invariably among algae, which dominate the life of a pond. It has been said that if all the higher plants in a pond were to be removed and replaced by glass models of the same shape and size, the animal life in the pond would go on just the same. Re­move the algae, and life would be vastly different. Knowing the number of parallels between the behaviour of frogs and the behaviour of algae, and that no two essential oils have the same chemical com­position or the same smell, I have always thought the hypothesis suffered from the difficulty of proof, rather than from any improba­bility. But there is no need to despair. After all, it was only in late 1957 that we had experimental proof that satellites were kept in their orbits by gravitation. Up till then the whole thing had been a hypo­thesis, based on a number of parallels! 

What Savage did not deserve was to be ignored by many of those who came after him. For example, in one chapter of a book published in 2005 which I will not name since it does not deserve even adverse publicity, Savage does not get a mention even though such factors as rainfall and odours in triggering spring migration in amphibians are discussed at considerable length. Like Trevor Beebee before me I find the omission of Savage—and not just in that one case—both astonishing and inexcusable.

However, all is not last since last week the popular BBC programme Countryfile included an item on frogs and a contributor said they were attracted to their breeding ponds by the smell of algae.

In the next article I will discuss how Maxwell Savage tried in his final research paper to take his algal hypothesis further but had to swap species in order to do so.

*the smell of Synura and the chemical composition of the odours produced is described in this YouTube video.

R Maxwell Savage: The Forgotten Doyen of British Ecological Herpetology Part 3: His 1961 Book on the Common Frog

Ronald Henry Maxwell Savage’s book, The Ecology and Life History of the Common Frog (Rana temporaria temporaria) was published in London by Pitman (1961) and in the USA by Hafner, New York in 1962. An online version of the USA edition can be found here; this version is also offered for sale as a ‘print’ version of bound photocopied pages with the claim that the work is in the public domain. With Savage having died in 1985, i.e. 36 years ago, the work is still, as I understand the law, under copyright in the UK and also I suspect in the USA.

It has proved an interesting exercise to re-read the book after first reading it more than than 55 years ago. I have also been able to compare my impressions with reviews written at the time. I am reproducing those reviews here because while recommending strongly that it should still be read by those working on amphibians as professionals or amateurs it is useful to consider what contemporary reviewers thought of it and its various strengths and weaknesses. I have found four reviews in searches; each has important things to say

The most extensive review was that written by Richard George ZWEIFEL (1926-2019) of the American Museum of Natural History for Copeia:

Dr. Savage has concentrated most of his research effort for more than 30 years on the ecology in the British Isles of this one species of frog. This book is in large part a compilation of the results of research reported in a series of papers that com­menced in 1935. although new data are presented and old data are in some instances re­-examined and reinterpreted. It is most worth while to have this published material and new information assembled in one narrative. 

The author's concept of ecology cuts across a broad spectrum of scientific disciplines and he is ready to delve into any subject that may illuminate some phase of the life of his chosen animal. Thus, illustrating his ap­proach. we find material on the biochemistry of the jelly of the frog's egg, experiments on the behavior of young tadpoles in relation to water deficient in oxygen, observations on the relationship of gut contents to growth rate in tadpoles (how much of what a tad­pole consumes is really food?), statistical in­vestigation of density of internal parasites as a measure of mortality (from causes other than parasites) in tadpoles, and an analysis of the relationship of direction of wind to the number of frogs migrating to the breed­ing ponds, to mention just a few of many topics lucidly presented. 

The book is arranged in ten chapters, nine of which treat various aspects of the ecology and life-history of the frog, beginning with eggs and young tadpoles and going lull cycle to breeding behavior. The tenth chapter discusses statistical and other methods of study. An appendix treats in detail statistical aspects of problems dealt with in earlier chapters and a second appendix consists of a glossary. 

The longest chapter of the book is devoted to investigation of the influence on the date of spawning of variables in the external environment. Voluminous data on spawn­ ing dates (collected by volunteer observers cooperating with the Royal Meteorological Society) were available to Savage, who ex­amined the data statistically for possible correlations of weather with variation in spawning dates at different localities and in different years. The weather data used are those recorded at Government weather sta­tions, but Savage is well aware that his ani­mals do not live in weather instrument shelters. He points out that as long as there is reasonably good correlation between varia­tion at the instrument site and in the ani­mal's habitat he can make statistically valid use of the available data. Erroneous inter­pretations are not likely to result, and only low correlations of weather and behavior will be obscured. Nevertheless, when Savage can cite temperatures of spawn as different as 15° and 2I.5°C on the same day in the same area (but in different ponds) one cannot help but wish that data had been gathered somewhat closer to the microhabitat of the animals. 

The analysis of single elements of weather in relation to spawning offered little enlightenment, for Savage observed in the field and confirmed over the calculator that neither rainfall nor temperature alone correlated closely with date of spawning. When he studied the effects of climatic variables act­ing together, however, he uncovered signifi­cant correlations. The data were analyzed by means of "Joint functional regression dia­grams,” three-dimensional graphs in which isophenes representing spawning dates mean­der across a grid with two weather vari­ables (chosen in various combinations from monthly mean temperature, monthly mean rainfall and percentages of possible sunshine) on the axes. These laboriously constructed diagrams illustrate well the complex inter­ actions of the various environmental influences and make it apparent why analysis of single factors gave meager results. 

Another chapter deals with food, hiberna­tion. and migration. Little space is devoted to food. Savage tabulates the stomach con­tents of 17 frogs and provides additional data from the literature to contrast the food of Bufo and Rana. The conclusion that differences in food habits between the spe­cies are related in part to habitat differences between frogs and toads—“they eat what hap­pens to be there”—is certainly sound, al­though the suggestion that “Anura in general are not indiscriminate feeders" may raise some questions, depending upon how broadly one interprets “indiscriminate." There is certainly little evidence for taxonomic discrimination. For example, a recent paper by Inger and Marx (Exploration du Parc Na­tional de l’Upemba, fasc. 64, 1961) shows that a majority of the African species they studied had eaten representatives of three or four phyla. Referring to Bombina variegata in captivity, Savage states “They reject mealworms." citing this as an instance of animals being most ready to feed on prey they are most likely to find in their natural habitats. But the Bombina I  have kept for several years, orientalis and bombina as well as variegata, would long ago have starved had they rejected mealworms. 

Savage presents some information on hiber­nation sites, hut devotes the bulk of the chapter to a discussion of migration to the breeding ponds and the hypothesis that the characteristic odor given a pond by its algal flora is detected at a distance and guides the frogs to the proper pond. No effective chal­lenge to this hypothesis has been made since it was first presented many years ago, and the evidence for similar phenomena in anadromous fish returning to the stream in which they hatched and for homing in newts adds credibility to the hypothesis. 

This is a stimulating book and the reader will find himself comparing the behavior of Rana temporaria with that of the frogs he knows, mentally testing Savage's explanation against the actions of other species. Parallels between the European species and its North American relative Rana sylvatica are partic­ularly striking. The paragraphs describing the relatively brief appearance of adult frogs at the breeding ponds very early in the year, the concentration of egg masses in a shallow, restricted part of the pond, the swarming of newly hatched tadpoles atop the disintegrating masses of jelly all could have been written about sylvatica. It is only when Sav­age tells us that temporaria avoids wooded areas that we note a marked difference from the habits of the wood frog. 

A facet of the work disappointing to me is the slight use made of the marking-recap­ture technique of study. Savage makes his feelings plain: "I believe that the animals being studied should receive as little inter­ference as possible, for as soon as one does anything to them, they are no longer ‘at home.' By all means use any laboratory methods to study the environment, but leave the animals themselves alone." One can deduce growth rates, movements and sur­vivorship bv a variety of ingenious methods, but the concrete evidence provided by marked animals is often best. Savage did utilise paper tags for temporary marking of some animals, and some of the data most interesting to me were derived from these ani­mals. One frog tagged in its hibernating pond was recaptured in a breeding pond and thus verified (as no other data could have) one source of the breeding population of this particular pond. 

The records of 52 tagged frogs in one local population prevent a fascinating picture of the fluctuating composition of that popula­tion during the breeding season. On any night the tagged males outnumbered the tagged females, sometimes by as much as six to one, and among tagged individuals there were almost twice as many males as females. Males tended to remain at the bleeding pond for several days in succession, or return after disappearing for one or more days, whereas females in this instance were not in attend­ance for more than one night. Savage tells us that the number of the sexes are about equal, so the unbalanced sex ratio probably merely reflects the male habit of spending several nights in the pond. (Tenacity can have its rewards: male No. A18 mated with different females three nights in succession.) 

Savage concentrated his study at the breed­ing ponds, and consequently offers very little concerning the life of the frogs during the period when they are neither breeding nor hibernating. A chapter only two pages in length covers the life of the juvenile frog. Estimates given of three to six breeding frogs per acre are based on the number of egg masses counted in the ponds, but we are not told how the author knew the extent of the area served by each pond. Surveys of a large number of ponds showed that no pond served as a breeding site every year. What happens to the frogs when a pond is de­serted? An intensive marking program might provide an answer. 

The author makes broad hut somewhat spotty use of the literature. Thus, as an ex­ample of geographic variation in embryonic temperature tolerance, he cites the work by Volpe on Bufo americanus but not the work of Moore on Rana pipiens. Again, he cites without critical comment a report that the eggs of a species of Rana have a thermal death point of 45°C. a figure far higher than reported for any anuran whose eggs have been adequately studied. A purely personal feeling, but one that I expect is shared by many readers, is a dislike for the abbreviated style of litera­ture citation used (probably favored by pub­lishers because of saving in type setting) and for grouping of citations at the close of each chapter. I much prefer to see titles cited in full and to have the references in one place. 

A brief review cannot do justice to the years of effort and enlightened inquiry that went into the research, nor can it touch on more than a few of the subjects explored in the book. Anyone interested in the ecol­ogy of amphibians will profit from reading it; I recommend it highly. 

The following was written for Journal of Animal Ecology by Thomas Townley MACAN (1910-1985) while at the Freshwater Biological Association:

It is a commonplace idea that a distribution map should not be studied unless something is known about the distribution of the collectors from whose data it is compiled. More novel per­haps is the suggestion that a general ecological work should not be studied without some know­ledge of the author. Dr Savage writes in the foreword that he has been working on frogs for 30 

years, his degrees and where he took them are set out on the page before, and that is all the information there is about him. What sort of job has he held during the 30 years? What facilities in the way of collaborators and apparatus did it provide? How much time was he able to devote to frogs? What influenced him to follow certain lines in preference to others? These are some of the questions that readers may ask. As this is a pioneer work of its kind, and ecologists may learn from what Dr Savage did not achieve as well as from what he did, answers would have been useful. 

The author has been chiefly concerned with the factors that affect the date and place of oviposition and the behaviour before and during the process, but in the course of the 30 years he has investigated many other aspects of the biology of the common frog. These observations, together with those, often few and unimportant, of other workers are the subject of the first eight chapters. How much remains to be found out is striking; that is not a disparagement of Dr Savage's achievement but a demonstration of the length of time that work of this kind takes. The distribution of the species is established, but no explanation of the limiting factors is yet available. It is known what tadpoles eat, but not from what they derive nourishment, which makes a gap in any discussion about the factors limiting sizes of populations. The sizes of adult populations and the factors that limit them are also in need of further study.


Not until about the middle of the book does Dr Savage reach the work which has been his main interest. Fig. 20 is a map of the British Isles covered with ‘isophenes', lines drawn through places where the spawning date is the same. In a small area of South Wales and of North Devon, and in the south of Ireland, spawning is in January; to be exact, before 30 January which is day 30. Spawning between days 31 and 40 is also confined to the south and west. Late spawning, between days 71 and 80, is a phenomenon of the east side of England and the midlands. The latest spawning, after day 100 (10 March), is in the Pennine area. Incidentally this map is not accompanied by any information about how the data was gathered, nor on how many observations each isophene is based. 

In general the earliest breeding is found in places with the highest rainfall. Temperatures near freezing-point a month before spawning are associated with early spawning at a lower rainfall than at higher temperatures. When the weather two months before spawning is examined, early spawning is found to be associated with temperature above 6°C and is not greatly affected by rainfall. Light also plays a part. It is surmised that these climatic factors react on the frog through one or several species of algae, an outburst of which stimulates spawning. Some readers will be disappointed to find that there is still this big gap to be bridged by theory only, but the author argues cogently in support of the line he has chosen to pursue.

I am not competent to pass an opinion on the joint functional regression diagrams and the statistical methods on which these conclusions are based, but my colleague, Miss C. Kipling, praises them. Anyone interested in the factors governing any regular event such as oviposition or emergence is likely to find Dr Savage's method worth study. 

There is a danger that some readers, put off by the incompleteness of the earlier chapters, will lay the book aside before they reach the author’s main work. On the other hand it is valuable to have this scattered information brought together in one place. Many will be grateful to Dr Savage for bringing it together, and he is to be congratulated on the amount that his own researches have contributed and on the fair way in which he has written about what is known and what is not known. 

The following review for The Naturalist appeared over the initials E.B. Since the journal was based in the University of Leeds I soon found that the reviewer was Edward BROADHEAD, then senior lecturer in zoology and an expert on psocids, insects on which my ignorance is total:

This book is an account of the research, carried out by the author as a recreation, on the ecology of the common frog. It covers all stages of the life history egg, tadpole, juvenile and adult frogs and much information is brought together on parasites, distribution and breeding behaviour. The section on the relation between spawning dates and weather in chapter 8 is new and of great interest, and a full account of the method used and of other statistical methods in chapter 10 adds considerably to the value of the book.

 The book is written in a chatty and enthusiastic style. The author's work is recorded in great detail and with a wealth of comment and discussion, but the book would have been improved by a better balance. The work of others is mentioned but never in the detail accorded to the author’s own papers, and very often the comment and discussion on some of the factual material presented is excessive, much space being given in some places to pure conjecture as, for instance, on pp. 79 et seq. where density dependence is discussed. 

Finally, my old friend ‘Amo’, Emmanuel Ciprian AMOROSO FRS (1901-1982), wrote the following for New Scientist. He, I think, had met Savage at Zoological Society of London meetings. Amo had recently worked on the ‘marsupial frog’ Gastrotheca marsupiata while professor at physiology at the Royal Veterinary College.

Maxwell Savage has been interested in the Common Frog and its tadpoles for a long time and he has courageously undertaken to write this account of their lives. Nor does he speak only as a compiler; his 30 years of research on the amphibia qualify him unusually well for the undertaking. The material is organized in 10 chapters and in these the student of behaviour should find as much of interest as the ecologist, for examples of observed be­haviour under a wide range of circumstances are given liberally. The general biologist should appreciate the information presented on reproduction, growth, mor­phology and like topics, while students of population may note outstanding factual contributions and unanswered questions alike. 

The author is at his best when he is talking about the riddle of migration and his claims for his algal hypothesis are modest. The book not only solves many of the mysteries surrounding the movement of the frogs to the ponds but is also replete with facts about their life history and behaviour. It is unfortunate, however, that only a small group of specialists will be able to profit properly from this work, as several defects reduce its value for a wider audience. The organization is loose and the more outstanding highlights of the re­searches are swamped in the telling by redundant detail; it is thus difficult to use the volume for reference. Furthermore, each section seems to be addressed to those who already know that field and its history rather thoroughly. Perhaps the author will reply that he intended his book for just such an audience. If so, it is a very limited one; and it may be questioned whether any­one with so great a grasp of the subject will not have made a similar synthesis for himself already. 

Altogether, while one familiar with Savage's work will find here little that is wholly new, there is a vigour and a modi­cum of fresh thought that is stimulating and as a summary of Savage's thinking the book is valuable. 

 I can add very little to those reviews other than to point out that while some of the discussions are  to modern eyes completely beyond their sell-by-date (matters physiological for example) and, as I remarked in the first article of this series, errors were made in drawing the statistical material together, the whole approach that Savage took (‘he is ready to delve into any subject that may illuminate some phase of the life of his chosen animal’, as Zweifel put it) shines through.

Savage did himself a disservice by not adding some biographical information and the circumstances under which he operated as a part-time herpetologist. While the research, like any other, has to be judged on its merits regardless of the circumstances of the person doing it, I do think some information would have added greatly to the interest in his work and to a much deeper appreciation of his devotion to his pursuit. I also think Amo hit the nail on the head by recognising the difficulty the average reader would have in reading the book and in implying that hard editing would have been of great benefit; there the publishers were amiss in not insisting on it. Savage, though, answered the question of who the book was intended for in the first paragraph of the Preface: ‘I wrote the book for myself’.

In the next article I discuss Savage’s big idea and the evidence he gathered.

Amoroso. EC. 1961. Book Review. The Ecology and Life History of the Common Frog by R. Maxwell Savage. New Scientist 12 (23 November 1961), 511-512.

EB. 1961. Book Review. The Ecology and Life History of the Common Frog by R. Maxwell Savage. The Naturalist 1961, 35.

Macan TT. 1962. Book Review. The Ecology and Life History of the Common Frog by R. Maxwell Savage. Journal of Animal Ecology 31, 398-399.

Zweifel RG 1962. Book Review. The Ecology and Life History of the Common Frog (Rana temporaria temporaria) by R. Maxwell Savage. Copeia 1962, 667-669.

The Frog Man. R Maxwell Savage: The Forgotten Doyen of British Ecological Herpetology Part 2

R. Maxwell Savage
from Beebee 2010

In my last post I described the work done by R. Maxwell Savage on the relations between local climate and weather on the time of annual spawning of the Common Frog, Rana temporaria, in Britain. I also noted that I was delighted to find that Trevor Beebee, who found reference to Savage’s often seminal work on amphibians lacking and information on his life absent, had launched an appeal for information. As a result a biography appeared in Herpetological Journal in 2010, 25 years after Savage’s death. More information on Savage’s professional life has emerged and it throws considerable light on the approaches Savage took in studying the Common Frog at all stages of development, from the formation and workings of frog spawn and the life of the tadpole to the triggers for breeding. 

There cannot be many scientists who have had papers in Nature for their amateur as well as their unrelated day job. For that matter, there cannot be many scientists who have received research grants from the Royal Society and a PhD for their spare-time pursuit. R. Maxwell Savage had all of these distinctions as well as the Stamford Raffles Award from the Zoological Society of London in 1967.

Ronald Henry Maxwell Savage* was born in Wood Green, London, on 2 May 1900, the third child of the company secretary of an explosives company. The Savage family had a coat of arms and Savage appears in Fox-Davies’s book, Armorial Families†. From Queen’s College Cambridge (1918-21) he graduated in Natural Sciences. He was a chemist and worked for his entire professional life, 1921-1965, for S. Maw Son & Sons at Barnet in Hertfordshire. Founded in the 1820s the company manufactured surgical instruments, medical kits, as well as common pharmaceuticals, at a large factory built when the form outgrew its London premises. eBay has products made by Maw: infant feeding bottles; bedpans; invalid cups; inhalers; toothpaste; surgical gear and bandages. Field dressings were supplied to British and allied forces and, from published papers, dressings were a particular concern to Savage from the 1930s to the 1950s. Some of the testing and improvement of surgical dressings was done in collaboration with surgeons at the London teaching hospitals. Means of sterilizing dressings, the performance of thrombin-containing dressings designed to speed up blood-clotting and improving the absorbency and holding capacity of dressings were the subjects of some of the papers Savage published in medical journals. He was also involved in the use of chlorophyll as a deodorant—a craze for a while in the 1950s when we had chlorophyll toothpaste, chewing gum, soap, shampoo, lotions etc. With arguments raging on the efficacy of some of these products Savage demonstrated, using proper test procedures and statistical analysis, that ‘chlorophyll on cotton pads does reduce the odour of decomposing blood, the probability of our results arising by chance being less than one in 2,000 million’.

Savage was, in short, the epitome of the brave new world of industrial research in the 1930s. 

His approach to the development and improvement of products, was quantitative, experimental and observational; it included bioassays, testing and quality control that depend on rigorous statistical treatment. It is these attributes that he carried over into his research in the field and in his home laboratory on the Common Frog and other amphibians. He did experiments and used statistical techniques on his field data that put him years ahead of his time—and in so doing probably made much of his work incomprehensible to biologists of the day. I can just imagine the expression on the faces of those who listened to the papers he gave at the Zoological Society in the 1930s. Members of the audience would not, to put it politely, have been familiar with the concepts he presented. It is perhaps not surprising that he complained that his work had been met with ‘polite incredulity’.

I have made a list of his publications from his day job and of those on his research on amphibians;  it is appended below.

In the 1939 Register, the emergency census taken as preparation for war, Savage was living with his wife and incapacitated mother at Derwent Avenue, Mill Hill. He is described as ‘Chemist: analytical and research. Works Manager: surgical dressings’. He was chief chemist for Maw Son & Sons. It was the field dressings made by Savage’s team that were issued to soldiers in the field as ‘First Field Dressing’ packs that could be brought out of a battledress pocket and applied quickly to a bullet or shrapnel wound. Maws supplied many of the field dressings, first aid kits and surgical dressings to military and civil defence organisations and it is clear that as Savage’s research on surgical dressings went on into the 1950s that he was seeking continuous improvement in the company’s products.

British Army First Field Dressing Pack
by S Maw Son & Sons

Savage wrote of how he first became interested—and how that interest was encouraged—in research on amphibians. As a young man he came back from a holiday in France with some Yellow-bellied Toads, Bombina variegata. He was encouraged by Hampton Wildman Parker (1897-1968) then in charge of reptiles and amphibians at the Natural History Museum in London to publish some of the observations he had made and to do more. Savage noted the incongruity of a taxonomist encouraging research which was far from taxonomic but Parker was a Cambridge graduate, like Savage, in natural sciences which included biological subjects and chemistry. It seems possible that they had met in Cambridge because Savage graduated in 1921 and Parker (although three years older) in 1923. The paper on B. variegata was published in 1932 in Proceedings of the Zoological Society (PZS), since retitled Journal of Zoology.

Throughout the 1930s and beyond he published a string of papers on the Common Frog, mainly in PZS. I will not dwell on what he did in this article since I shall write follow-ups on specific aspects, including his book which pulled together his earlier work, as well as on his main hypothesis which occupied much of his time over the next 40 years.

This might though be a good place to put his huge amount of fieldwork in context. In his words:

The area lay on the borders of Middlesex and Hertfordshire, and covered about eighty square miles. Within this area 92 ponds were kept under observation over a period of ten years. None were observed for the whole of this time, for most of the observations were made between 1934 and 1938, although less systematic observations were maintained for another twenty years afterwards, and some of the ponds were known for twenty years before.

The ponds were within driving distance of where he lived, first in Mill Hill and then Hadley Wood.

The approximate area containing the 92 ponds studied by Maxwell
How many survive?

His work on tadpoles was written up for his University of London PhD thesis, The Ecology of Anuran Tadpoles, at Birkbeck College. The date given in the library catalogue is 1950-1951.

Both Savage and Louis Lantz were industrial chemists who worked, as amateurs, on herpetological matters in England. It is evident from Savage’s papers that they were in regular contact. Indeed, Savage collected Painted Frogs for Lantz on the French island of Port-Cros. He was in regular contact with Burgess Barnett—with whom he shared an interest in the mechanism of blood clotting—over the solidification of frog spawn after laying. We also know that Deryk Frazer helped him with summarising phenological data. When Savage was looking at the feeding mechanisms of tadpoles, Laurence Cooper Stuart (1907-1983) of the University of Michigan sent him specimens of a microhylid. Other names are mentioned in his book and it is clear that he was connected with all the key players in his areas of interest, in his ‘amateur’ as well as in his professional life.

Savage thanked his wife, Violetta, née Hetherington, whom he married in 1931 for helping him with fieldwork in the 1930s; they were married in 1931. He also thanked a Dr W.F. Purdy (also acknowledged in one of his papers from Maw Son & Sons) for help with transport and advice on presentation of the figures, and a Mr A. Edwards; I have been unable to find any information on either.

Trevor Beebee mentions that Savage from the 1920s onwards travelled widely on holidays in continental Europe. The fire-bellied toads from France I mentioned above which started his research activity were one obvious result of his travels as were the painted frogs sent to Louis Lantz.

Savage was a Fellow of the Royal Institute of Chemistry and of the Zoological Society of London. He became a member of the British Herpetological Society soon after its foundation in 1947, and was one of my predecessors as editor of its journal, the British Journal of Herpetology (now Herpetological Journal).

On retirement the Savages moved from Hadley Wood to Welwyn where Ronald Maxwell Savage died in 1985.

In the next article in this series I will discuss his book and its reception before moving on to discussion of his big idea, some of his earlier research and of his studies on Xenopus.

†Argent, on a fesse dancetté between four lioncels three in chief and one in base sable, two doves each holding in the beak a branch of olive proper. Mantling sable and argent. Crest—On a wreath of colours, in front of a lion’s jamb couped or, grasping a branch of holly fructed proper, a saltire sable. Motto—“A te pro te”. That coat of arms (a variant of those by branches of the Savage family) appears to have been granted to Henry Maxwell Savage (1861-1938) in 1918.

*He seems to have dropped H[enry] from his initials; he always published under the name R. Maxwell Savage.

Beebee TJC. 2010. Ronald Maxwell Savage, 1900-1985: a tribute. Herpetological Journal 20, 115-116.

Ronald Henry Maxwell Savage

Publications and Radio Broadcasts

Herpetology

Note that the volume numbers of Proceedings of the Zoological Society are ones currently listed on the ZSL publication website. Various other methods of numbering the volumes were used in the past and may be encountered in Savage’s own papers and book.

Savage RM. 1932. The spawning, voice, and sexual behaviour of Bombina variegata. Proceedings of the Zoological Society of London 102, 889-898.

Savage RM. 1934. The breeding behaviour of the common frog, Rana temporaria temporaria Linn., and of the common toad, Bufo bufo bufo Linn. Proceedings of the Zoological Society of London 104, 55-70.

Savage RM. 1935. The influence of external factors on the spawning date and migration of the common frog, Rana temporaria temporaria Linn. Proceedings of the Zoological Society of London 105, 49-98.

Savage RM. 1935. The ecology of young tadpoles, with special reference to some adaptations to the habit of mass‐spawning in Rana temporaria temporaria Linn. Proceedings of the Zoological Society of London 105, 605-610.

Savage RM. 1937. The ecology of young tadpoles, with special reference to the nutrition of the early larvae of Rana temporaria temporaria Linn., Bufo bufo bufo Linn., and Bombina variegata variegata Linn. Proceedings of the Zoological Society of London 107, 249-260.

Savage RM. 1939. The ecology of young tadpoles, with special reference to carbohydrate changes in development, and to the function of the envelope. Proceedings of the Zoological Society of London 108, 465-480.

Savage RM. 1939. The distribution of the spawn-ponds of the common frog, Rana temporaria temporaria Linn., over a portion of the London clay and associated drift. Proceedings of the Zoological Society of London 109, 1-19.

Savage RM. 1942. The burrowing and emergence of the Spade‐Foot Toad, Pelobates fuscus fuscus Wagler. Proceedings of the Zoological Society of London 112, 21-35.

Savage RM. 1950. Observations on some natural epizootics of the trematode Polystoma integerrimum among tadpoles of Rana temporaria temporaria. Proceedings of the Zoological Society of London 120, 15-37.

Savage RM. 1952. Malcolm Smith (1951). The British Amphibians and Reptiles [book review]. Journal of Animal Ecology 21, 162-163.

*Savage RM. 1952. Ecological, physiological and anatomical observations on some species of anuran tadpoles. Proceedings of the Zoological Society of London 122, 467-514.

Savage RM. 1955. The ingestive, digestive, and respiratory systems of the microhylid tadpole Hypopachus aguae. Copeia 1955, 120-127.

Savage RM 1956. Thermal function of the envelope of the egg of the common frog Rana temporaria, with observations on the structure of the egg clusters. British Journal of Herpetology 1, 57-66.

Savage RM. 1961. The Ecology and Life History of the Common Frog (Rana temporaria temporaria). London: Pitman.

Savage RM. 1963. A speculation on the pallid tadpoles of Xenopus laevis. British Journal of Herpetology 3, 74-76.

Savage RM. 1965. External stimulus of the natural spawning of Xenopus laevis. Nature 205, 618-619.

Savage RM. 1971. The natural stimulus for spawning in Xenopus laevis (Amphibia). Proceedings of the Zoological Society of London 165, 245-260.

*Footnote to this paper: This paper has been condensed from part of a thesis approved by the University of London for the degree of Ph.D

Professional

Savage RM. 1936. Penetration of heat into surgical dressings. Chemist and Druggist 125(2943), 14.

Savage RM, Chambers WP. 1938. Optimum temperature of formation of a blood clot. Nature 141 287-288.

Savage RM. 1940. Sterility tests on surgical dressings. Quarterly Journal of Pharmacy and Pharmacology 13, 237-251.

Savage RM. 1942. The sterilization of paraffin surgical dressings. British Medical Journal 1942(1), 472-474.

Savage RM. 1944. The sterilising action of steam admixed with air and other gases. Chemist and Druggist 142(3362), 73.

Savage RM. 1945. The sterilisation of surgical dressings. Pharmaceutical Journal 1945, 254.

Chambers WP, Savage RM. 1945. A comparison of methods of analysis of euflavine gauze with observations on the effect of sterilisation. Quarterly Journal of Pharmacy and Pharmacology 12, 237-234.

Savage RM, Bryce DM, Elliott JR. 1952. The water retention coefficient of surgical dressings. Journal of Pharmacy and Pharmacology 1952 4, 944–958.

Bryce DM, Savage RM. 1953. A note on surface-active agents and surgical dressings. Journal of Pharmacy and Pharmacology 5, 911-915.

Bryce D, Savage RM. 1953. Chlorophyll. British Medical Journal 1953(1), 833.

Savage RM. 1954. The sterilization of surgical dressings. Journal of Applied Bacteriology 17, 278-285.

Savage RM. 1954. A statistical study of variation in surgical dressings. Journal of Pharmacy and Pharmacology 6, 843-858.

Savill A, Daynes G, Savage RM. 1956. Bread. Lancet 267, 1071.

Savage RM. 1957. Sterilization of dressings. British Medical Journal 1957(2), 235.

Savage RM. 1962. Sweetened dummies. British Medical Journal 1962(2), 801.

Radio Broadcasts

3 February 1956. Naturalists’s Notebook. Edited by Maxwell Knight. Produced by Brandon Acton-Bond

8 March 1959. The Naturalist. BBC Home Service. Introduced and edited by Maxwell Knight. Produced by Jeffery Boswall