Tuesday, 23 March 2021

Frogs: Climate and Spawning. R Maxwell Savage: The Forgotten Doyen of British Ecological Herpetology Part I

Frogs in Ayrshire were spawning last week, a few days before World Frog Day 2021 but unchanged over the past 40 years. Continuing the theme of what external events trigger amphibians to breed, I wondered what had happened further after the extensive research of R. Maxwell Savage on the Common Frog, Rana temporaria in Britain from the 1920s to the 1950s. Savage was something of a mystery man as far as I was concerned. Not only to me I discovered because I was delighted to find that Trevor Beebee had found himself in a similar position. Trevor appealed for information and the result was contact with the Savage family and a short biography in a 2010 issue of Herpetological Journal. I will return to Savage’s life and achievements in a later post but I should say now that I have him down, using my grandsons’ terms, as a super-hero in British herpetology.

I remember reading Savage’s book, The Ecology and Life History of the Common Frog (Rana temporaria temporaria) rather quickly around 1963-64, three years after it was published; quickly because it had to be returned to the library. However, I do remember being aware that one of its main conclusions, that earlier spawning is associated with higher rainfall in the month or so before the actual event, I knew of before then. But how did I know and how did the person who told me know when I could remember being told the story before the publication of Savage’s book in 1961?

Some conversations and their locations stick in the mind while other events disappear from the memory banks. In summer 1959, several of us were in the Junior Biology Lab of the former and now completely demolished Henry Mellish Grammar School and with nothing much to do after taking ‘O’ levels were surveying the biodiversity (in modern terminology) of the school pond. We were talking about tadpoles and frogs when the senior biology master James John Key, who died in 1976 at the young age of 59, told us the story he had picked up about rainfall and spawning. Only when I was doing online searches on Savage did I remember how Jim Key had found out: Ronald Maxwell Savage was on the BBC Home Service radio programme The Naturalist on 8 March 1959. In the programme, edited and introduced by Maxwell Knight, ‘R. Maxwell Savage shows how the spring emergence and spawning of the common frog are stimulated by changes in the weather’ (Radio Times 5 March 1959).

Jim Key listened to that programme and to others on science, not only to keep himself informed of developments but as a source of ammunition for his arguments in the staff room with Stanley Revill, the senior history master, antiquary and archaeologist, who would ask provocative questions in order to stimulate conversation on weightier matters than who had last used the ink eradicator. For example, both listened to P.B. Medawar’s Reith Lectures in 1959, The Future of Man. By this time I was in the Lower VIth and Jim would appear, looking for arguments against (preferably) or for Stan’s latest pronouncement. ‘Natural selection has ended’ was one that kept us going right to the staff room door as Jim re-entered the fray.

After that digression, I want to consider what Savage had done that led him to the conclusion on the importance of rainfall. In Britain spawning date varies with geographical location and from year to year. Savage tried to determine the cause of these variations. It was only a part of his research on the Common Frog but it is an interesting one—and an important one given the effect of climate and weather on natural events. His paper was published in 1935 but he expanded on that exercise in his 1961 book.

Savage’s study of the spawning date of Common Frogs was an exercise in phenology—the study of the times of recurrence of natural phenomena and in particular the influence of climate on plants and animals. Britain has long been obsessed by such events as hearing the first cuckoo in spring or the first flowering of a plant. An enormous ‘citizen science’ project ran between 1891 and 1948 organised by the Royal Meteorological Society with up to 600 recorders submitting returns in some years. Each year a Phenological Report appeared. In the earlier years, the date of frogs spawning was reported but not included in the annual report. Savage searched the individual returns so that he had as complete a set of data as possible.

Savage produced this map from his analysis of phenological reports

Savage then extracted seven meteorological readings from the Monthly Weather Reports compiled by the Meteorological Office. This was a massive task and he received special permission to borrow each volume of reports to work on at home during the evenings and weekends. In these days before computers, Savage entered the data by clipping punched cards (2,734 in all) and then sorted them for each variable by passing a needle through the relevant hole and allowing those clipped to fall out of the stack. In that way, the standard method in statistical operations of the time, he built up tables for analysis and ‘joint functional regression diagrams’.

The diagrams he produced need a little explanation. He was able to plot on a graph, with average monthly rainfall and average monthly temperature as the axes, points at which spawning occurred on certain dates (expressed as day of the year, eg 1 January = 1 etc). He then joined equal dates of spawning with a line—an isophene—analogous to an isobar on a weather map. Each diagram then had a family of isophenes ranging from early spawning (day 20, i.e. 20 January) to very late spawning (day 90, 31 March).

To digress for what he would have obtained had the date of spawning been simply associated with temperature or rainfall, I show theoretical diagrams below. In each case the isophenes would be parallel to one axis or the other. But Savage did not obtain isophenes parallel to an axis. The isophenes were curved showing a complicated relationship between temperature, rainfall and spawning date.

Savage's Diagrams showing isophenes of day of spawning.
The shades areas are where there we no data

Savage’s significant contribution was to look at the patterns of rainfall, temperature and spawning not just in the month of spawning but in each of the two months before spawning. However, he then hit a problem because the usual month of spawning was not the same throughout Britain, as his map showed, and was sometimes variable from year to year in any one region. Therefore for each record he designated the month of spawning as M0, the previous month as M1 and the month before that as M2. The reader of his book can be confused by this notation because it would have seemed more logical to denote the month before breeding as M-1 etc.

He had to use months as the unit because the meteorological records were presented as averages for a particular month. That made his conclusions for the month of spawning, M0, potentially less valuable as he explained: 

It is obvious that the weather near the end of M0 cannot affect the actions of frogs spawning at the beginning, and, for that reason, the use of a mean value for this month must introduce errors. It is, however, a property of the weather that it runs in spells, so that the Meteorological Office can head its monthly reports with a condensed summary in a short phrase, such as “Warm in the west, colder and windy in the rest of the country”. The mean values used in this work are therefore not so bad a measure as would appear at first sight.

Savage went into considerable detail in attempting to interpret the three diagrams. I will limit what follows. In general, in the month of spawning (M0), early dates for spawning are associated with higher rainfall; both relatively and high and relatively low temperatures with low rainfall are associated with later spawning. A similar conclusion can be reached about the month before spawning (M1). By contrast, two months before that of spawning (M2), temperature is far more important, higher temperature being associated with earlier spawning. An effect of rainfall is still present particularly at lower temperatures.

It is the marked association of rainfall in the preceding month or so with the date of spawning that Savage talked about on the BBC in 1959.

Savage demonstrated clearly an association between rainfall and spawning date, an association stronger at that time than the effect of temperature. It doesn’t need stating that demonstration of an association is not a demonstration of causation or that rainfall is not a proxy for some other event associated with high rainfall. However, the shift in spawning date seen after the extremely cold winter of 1947 (with ponds frozen until after day 70) argues in favour of an effect of, at least, severe changes in environmental conditions. In 1940-46 in south-west England the average day of spawning was 36 (5 February); in 1947 it was 77 (18 March).

Ecologists have often seemed reluctant to embrace experiment (a criticism that does not extend to Savage) and as far as I have been able to determine, there has been no experimental test of the effect of rainfall and temperature on the date of spawning. If, say, frogs from parts of the east of Scotland or of east Anglia (regions with late average spawning dates) were moved to Cornwall would they conform to the early spawning date observed there?

Savage thought he knew why higher rainfall is associated with early spawning and how the effect is brought about. This is an important I shall return to in a future article since it is a theme that runs through all Savage’s observations and research.

Ronald Maxwell Savage spent an enormous amount of his time—months of work he stated—in pre-computer days on extracting the data, preparing the data for analysis and doing the final statistical calculations. He thanked ‘Dr Frazer’ [John Francis Deryk Frazer, 1916-2008] for copying out the spawning dates from the Phenological Reports. Therefore, I find it odd that Deryk Frazer made so little of the approach or of Savage’s findings, confining the inadequate description to a short paragraph, in his Reptiles and Amphibians in Britain which was  published in 1983 in the New Naturalist series,. Perhaps I should not have been too surprised because in the same volume he also misinterpreted Savage’s later work.

As well as producing his diagrams, Savage, a skilled exponent of statistical analysis for reasons I will explain in a later article, used multiple regression analysis on the meteorological, location and spawning date data in order to determine the influence of individual factors. In addition to rainfall and temperature he included altitude, latitude, longitude and hours of bright sunshine. From this analysis he obtained a multiple linear correlation coefficient of 0.74, remarkably high, he suggested, for such data; I agree. That would account for just over 50% of the variation in spawning data observed and, as Savage observed, could well be an under-estimate for reasons he explained.

I thought I would try, using Savage’s multiple regression equation that he showed in his book, and average local data to see if it produced a spawning date in the right ball park. However, I soon realised that one term (temperature in M2) was missing entirely and the coefficients for latitude and longitude seemed 10x out. Using the equation as it is shown produced nonsensical answers. Unfortunately, I have found no reference to its use by others nor to its obvious errors which must have occurred during conversion of units, copying or type-setting. If it were usable it could have provided a valuable tool to test the effect of increasing environmental temperatures on spawning date (see below) and how well it corresponded to current data on climate and spawning dates. It is unfortunate that the absence of ‘hard’ editing is often evident in Savage’s papers as well as in his book. There are some obvious errors as well as the reader—well this reader—being left puzzled by what seems to be an error, omission or lack of explanation. One example is that the beta coefficients shown in the regression equation on page 143 (with one missing) are not the same as shown in Table 7 on page 145.

Savage also showed the beta coefficients obtained in his regression analysis (i.e. the slope, negative or positive, for each component). He used their relative size to estimate the main factors. Retarding influences (i.e. later spawning dates) were associated with higher temperature in M0; increase in latitude; increased sunshine in M1. Accelerating influences were: increase in longitude; raised temperature in M2; increased rainfall in M1. These conclusion can, of course, also be deduced from his diagrams.

Therefore, In any one location from year to year, the effects of geography removed and the list of influences can be shortened. Retarding are: increased sunshine in M1; high temperature in M0. Accelerating are: high temperature in M2; increased rainfall in M1. However, this could not be the whole story since, as Savage observed, although some ponds were near together the frogs spawned at different times. Again, I will return to how Savage explained the differences in a later article.

Savage appreciated the importance of an effect on winter temperature (i.e. in M2) on spawning date and its compatibility with what was known about frog physiology. Gametogenesis is temperature dependent and Trevor Beebee found that between 1979 and 1994, although spawning date did not change significantly over that period at a single site, there was a strongly negative correlation with overall winter maximum temperatures*.

It would seem that the tradition of making rather little of Savage’s extensive work and statistical analysis, as exemplified by Frazer’s book and pointed out by Trevor Beebee, lives on. For example, in a recent paper on the possible effects of climate change on breeding in the Common Frog, Savage is mentioned but only in respect of noting that spawning dates may be different in ponds in the same area. Completely ignored in this new phenological analysis across a number of sites from 1994 onwards was the importance of the timing of rainfall in the months before spawning as found by Savage and the acceleration of spawning by higher temperatures in M2 but a retardation of spawning with high temperatures in M0. There was incidentally, no statistically significant trend for spawning dates to be earlier, although there was a tendency in that direction. The plot of spawning day versus year would have been dismissed by a late colleague as just ‘a swarm of bees’. Savage may have been wrong—or right—in his conclusions but his findings have to be explained in the light of further evidence, not ignored, as well as being taken into account in designing statistical procedures to analyse changes with time.

Finally, and with more on Ronald Maxwell Savage to come, the original data sources still exist. Somebody could re-extract the information, which would be time consuming but the months spent on statistical analysis—which could go much further than even Savage could crank out by hand—would be reduced to minutes. Given the importance of determining the effect of anthropogenic warming, these historical phenological records could be of much greater significance than Savage could ever have anticipated.

Beebee TJC. 1995. Amphibian breeding and climate. Nature 374, 219–220. 

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. 1961. The Ecology and Life History of the Common Frog. London: Pitman.


Tuesday, 16 March 2021

The Mouse Adrenal X-Zone Revisited


This photomicrograph (from here) shows the cross section of a female mouse.
The medulla (M), X-zone (XZ) and zona fasciculata (ZF) of the cortex are labelled.
The outer, zona glomerulosa, of the cortex can be seen but is not labelled 


For a few months in 1965-66 I worked on the aptly-named X-zone of the mouse adrenal in Hong Kong. In 2018 I wondered what had happened to research on the X-zone. Had its function been discovered? The answers were in fact ‘rather little’ and ‘no’ and so I offered to give a talk at an annual Society for Endocrinology meeting in an attempt to stir up some interest in a problem that has intrigued those interested in the workings of the adrenal gland since the 1920s. This I did in November 2019 at Brighton meeting of the British Endocrine Societies.

I have written below an account of the cellular origins of the X-zone because it now transpires that we were misled in the 1960s by the misinterpretation or misreporting of early findings and that, in fact, the early workers were right about where it came from during development of the embryo. In addition, nobody it seems had spotted an important paper published in 1942 that made our experiments in Hong Kong unnecessary. But first the personal historical background:

Four weeks after we had arrived in Hong Kong, I received an aerogramme from John Phillips he had written on 28 November 1965. He was on his first ‘long leave’ from the University of Sheffield and was spending it back in Sheffield with Ian Chester Jones, where, until December 1962 he had been a lecturer. We had been up to Sheffield several times before leaving for Hong Kong on 1 November and the general idea was that I should have a look to see if steroid hormones found in vertebrates occur in invertebrates as well. I was beginning to see what we had in terms of chromatographic equipment and chemicals in order to make a start when that aerogramme arrived. He wrote:

…I listened to Prof Paul Delost give a lecture on the X Zone last night and I was surprised to hear that he considers the X zone to be under medullary control. He bases this conclusion on the absence of an X zone in an adrenal in which the medullary tissue has been aspirated from the centre of the gland with a needle and vacuum pump—the other gland remaining as a control. The interesting thing about this preparation is that if you castrate the post-pubertal male the X zone reappears in the gland with a medulla but not in the other adrenal without a medulla…But the main criticism of Delost’s approach is that he destroys the vascular bed of the adrenal. This can be overcome by an operation called “enucleation” in which the whole of the adrenal is expressed leaving only the capsule from which a new adrenal cortex regenerates. Will you get some male mice and enucleate adrenals before puberty…

That I did and the results were clear. Given though the techniques available at the time it was difficult to envisage taking the approach further. The caravan moved on.

Cellular Origins of the X-Zone

After its description1 but misidentification in 1924 by Kiyoshi Masui and Yasushige Tamura of the Imperial University of Tokyo (with a further publication in English in 19262) and  its naming in 1927 to reflect its unknown function by Evelyn Howard (1904-1999) then at Stanford3, the X-zone of the mouse adrenal excited the interest of pioneering endocrinologists who did not yet describe themselves as such. The structure, which develops after birth between the cortex proper and the medulla, still befits its name; the function of the X-zone remains unknown4,5. Early work was concerned with its origins and with its hormonal control since it disappears at puberty in males and during first pregnancy in females6.

In terms of hormones in the circulation, androgens cause the X zone’s disappearance while LH (luteinising hormone) from the pituitary is necessary for its maintenance4,7. Although excellent research was done in the early years on the possible cellular origins of the X-zone it is only more recently that cell lineage studies using molecular markers have provided further evidence that it is derived from the fetal or inner adrenal cortex, as opposed to the definitive or outer cortex which forms the well-known zones of the adrenal: glomerulosa, fasciculata, reticularis (references in4). Therefore, the X-zone of the mouse appears to be homologous with the human fetal adrenal cortex, which, as its names implies is present only in the developing fetus. Such an origin was suspected by some early workers who referred to the ‘human fetal X-zone’ but strongly denied by others. Other possible homologues are the juxtamedullary zones of various size and appearance observed in some other eutherian mammals (cat, rabbit, voles, hamsters, and shrews)6,8.

In this short article I first consider whether the more modern findings on the origins of the X-zone are consistent with the early studies since the over-riding impression created in the mind by reading reviews and papers from the latter half of the 20th century is that the X-zone is derived from the inner cells of the zona fasciculata or, in other words, is just another zone of the definitive cortex. Then I review the evidence from little-known perturbative experiments, published, to modern eyes, in obscure places, that throw light on the origins of the X-zone.

That the X-zone is derived from the fetal or inner cortex is entirely consistent with the findings of Harry Waring9 who was then working in Liverpool for an M.Sc. The topic was suggested to him by a forgotten promoter of endocrinology in Britain, a famed lecturer in zoology, Ruth Culshaw Bamber (1889-1970) who was always known as Mrs Bisbee.  Horace ‘Harry’ Waring (1910-1980) showed in 1935 that during embryonic development there is—initially—an intermingling of the cortical and medullary elements. Remodelling then concentrates the medulla until there is a clear separation from the cortex. He identified cells, comprising what he called the interlocking zone, between the medulla and cortical elements. These cells became concentrated around the time of birth into a layer around four cells thick. The outer cortex in the meantime was growing and forming the usual zones. But it was that layer of interlocking cells that went on to form the X-zone after birth. Later, as the X-zone degenerated there was left a ‘medullary connective tissue capsule’ or ‘juxtamedullary capsule’ around the medulla formed, it was presumed, from the collapsed stroma9.

In 1928, Ruth Deanesly (1901-1997) in London had already observed that after degeneration of the X-zone some of its cells remained around the juxtamedullary capsule10. Therefore, the key early finding that a secondary X-zone forms after castration of male mice can be explained by growth from these cells, i.e. remnants, capable of division, of an inner (fetal) cortex rather than from a differentiation of cells from the inner zone (z. fasciculata in the mouse) of the outer (definitive) cortex.

I cannot explain why the view prevailed, despite evidence to the contrary, that the X-zone was part of and derived from the outer or definitive cortex. As one example, the following is from the highly influential review written by Helen Wendler Deane (1917-1966) published in 19628, four years before her early death:

These [X-zone] cells differentiate postnatally, at about 2 weeks, from the inner portion of the fasciculata (Whitehead 1933a, Waring 1935).

The problem with this statement is that neither Raymond Whitehead11, working in Manchester, nor Harry Waring9 drew any such conclusion. Only Waring of the two studied the origins of the X-zone and his conclusion was, as I have noted above, entirely different.

All the above evidence, even the sophisticated and relatively recent cell lineage studies, have been observational. Those seeking direct, experimental evidence that throws light on the origin of the X-zone would at first sight be discouraged since it all appeared over 50 years ago in obscure publications and/or written in French while one important paper had, I discovered recently, been overlooked entirely.

Until I found that paper, the first experimental work that has a bearing on the problem was thought to have been that in the 1960s from Paul Delost’s laboratory at the University of Clermont-Ferrand in France and in particular that of his student Parviz Chirvan-Nia who later returned to Tehran University of Medical Sciences in Iran. They took advantage of the fact that a secondary X-zone develops after castration in male mice. Their most pertinent finding12,13 was obtained in mice from which the adrenal medulla had been removed by aspiration through a very fine pipette, a technically difficult procedure. In males in which the entire medulla had been removed, a secondary X-zone failed to develop after castration. By contrast, if even a small piece of medulla remained, an X-zone developed around it. The effect was local; the untreated contralateral adrenal was unaffected.

All of Delost’s work from the 1950s onwards was published in French and had received little attention in the English-speaking world. However, on 27 November 1965 Delost was invited by Ian Chester Jones (1916-1996) to give a seminar in Sheffield, having been one of Chirvan-Nia’s external examiners earlier that year. His old student, John Guest Phillips (1933-1987; FRS 1981), on leave from the University of Hong Kong, was also there and while intrigued by Delost and Chirvan-Nia’s work he and Chester Jones were concerned that, in aspirating the medulla, the venous drainage from the adrenal would have been destroyed. They thought that a complementary approach, that of enucleation, in which end of the adrenal is snipped off and the medulla and most of the cortex squeezed out, would be a useful test. After enucleation the outer cortex redevelops and shows a normal zonation but without a medulla. As a result, John Phillips sent me an aerogramme the next day asking if I, having arrived in Hong Kong four weeks earlier as a PhD student, would take it on. This I did and the results were identical to those obtained by Chirvan-Nia and Delost: a secondary X-zone failed to develop if the medulla had been removed completely; if even a small remnant of medulla remained after incomplete enucleation, an X-zone developed around it14.

In 2019 while preparing a talk5 for the Society of Endocrinology on what has happened to research on the X-zone I discovered our experiments had simply confirmed what had already been published. The same approach, enucleation, had yielded the same results in 1942. The paper, which appears not to have been quoted by anybody working in or reviewing the field, was by Murchie Kilburn McPhail (1907-1987) and his student H.C. Read, of Dalhousie University in Canada15. I can only assume that it was missed because it appeared in wartime, albeit in a leading journal, when scientists were otherwise occupied. However, another paper from the same authors from the same year was picked up and referred to.

Suggestions as to possible mechanisms as a result of these experimental approaches, for example what would now be termed a paracrine effect of medullary cells on the inner cells of the  cortex against the direction of blood flow, can now be discarded since the removal of the medulla would by any technique result in the extirpation of the inner cortical anlagen formed in and around the juxtamedullary connective tissue capsule after degeneration of the X-zone.

In conclusion, the original observations by Harry Waring on the origins of the X-zone and the experimental evidence on the necessity of the adrenal medulla for the presence of an X-zone are entirely consonant with the X-zone being derived from the fetal or inner cortex and not the definitive or outer adrenal cortex. The recognition that there are two populations of cortical cells only one of which is responsible for the classical zonation of the adult adrenal gland explains many of the false leads followed, blind alleys entered and bold assertions made by those working in the field during the middle decades of the 20th century.

Research over the past 96 years has established the hormonal control of the adrenal X-zone and seemingly settled its cellular origins. Will we also know its function by the time of the centenary of its discovery?

1. Masui K, Yamura Y. 1924. The effects of gonadectomy on the structure of the suprarenal glands of mice, with special reference to the functional relation between this gland and the sex gland of the female (Translated). Nihon Chikusan Gakkaiho 1, 55–79.

2. Tamura Y. 1926. Structural changes in the suprarenal gland of the mouse during pregnancy. Journal of Experimental Biology 4, 81–92.

3. Howard E. 1927. A transitory zone in the adrenal cortex which shows age and sex relationships. American Journal of Anatomy 40, 251-293.

4. Huang C-C J, Kang Y. 2019 The transient cortical zone in the adrenal gland: the mystery of the adrenal X-zone. Journal of Endocrinology 241, R51–R63.

5. Peaker M. 2019. What happened to the adrenal X-zone. Endocrine Abstracts 65 SE 1.1. DOI: 10.1530/endoabs.65.SE1.1.

6. Chester Jones I. 1957. The Adrenal Cortex. Cambridge: Cambridge University Press.

7. Gannon A-L, O’Hara L, Mason JI, Jørgensen A, Frederiksen H, Milne L, Smith S, Mitchell RT, Smith LB. 2019. Androgen receptor signalling in the male adrenal facilitates X-zone regression, cell turnover and protects against adrenal degeneration during ageing. Scientific Reports 9, 10457.

8. Deane, H.W. 1962. The anatomy, chemistry, and physiology of adrenocortical tissue. In The Adrenocortical Hormones Part 1. Handbuch der Experimentellen Pharmakologie, edited by Eichler O & Farah A, subedited by Deane HW, 1-185. Berlin, Springer.

9. Waring H. 1935. The development of the adrenal gland of the mouse. Quarterly Journal of Microscopical Science 78, 329–366.

10. Deanesley R. 1928. A study of the adrenal cortex in the mouse and its relation to the gonads. Proceedings of the Royal Society B 103, 523–536.

11. Whitehead R. 1933. The involution of the transitory cortex of the mouse suprarenal. Journal of Anatomy 67, 387–392.

12. Chirvan-Nia P. 1965. Données nouvelles sar la zone X surrénalienne de las souris. Doctoral Thesis, Université de Clermont.

Brudieux R., Chirvan-Nia P., Delost P. 1966. Sur les relations directes entre la médullo-surrénale et le cortex surrénal. Journal de Physiologie, Paris 58, 213-217.

14. Peaker M, Phillips JG,. Peaker SJ. 1967. A relationship between the medulla and the X-zone of the mouse adrenal. In Proceedings, Third Asia and Oceania Congress of Endocrinology, edited by Litonjua A, vol. 2 317–321. Manila.

15. McPhail MK, Read HC.  1942. Regeneration of adrenal gland following enucleation and transplantation with special reference to X-zone. Endocrinology 31, 486–492.

Saturday, 20 February 2021

Frank Evers Beddard: Descriptive zoology at the turn of the 20th century

Frank Evers Beddard

Those browsing in public libraries in the middle of the 20th century would be excused, I hope, since I was one of those browsers, for gaining the impression that F.E. Beddard’s life’s work had been on mammals. Libraries sometimes had on their shelves volumes in the Cambridge Natural History, a series of ten volumes published, out of numerical order, between 1895 and 1909. Beddard wrote volume 10 in 1902; it was on mammals.

It seemed obvious that Beddard was a specialist in mammals; at the time he wrote it he was Prosector to the Zoological Society of London, and London Zoo had lots of dead mammals each week to work on. However, he made his name on an entirely different group of animals, earthworms, the oligochaetes.

Frank Evers Beddard was born in Dudley in 1858, the son of a prosperous businessman. Educated at Harrow and Oxford (graduated 1880) he was appointed to work on the animals collected by the Challenger Expedition of 1872-1876, involving a circumnavigation of the earth for oceanographic research. The job was in Edinburgh and he was assigned the isopods to describe and identify; his results were published in two of the 50 volumes, a marathon of descriptive zoology. In Edinburgh he also began to take an interest in earthworms.

A plate from Beddard's report on isopods
collected by the Challenger Expedition

Beddard was appointed to the prosectorium at London Zoo in 1884. At that time Philip Lutley Sclater was Secretary (i.e. chief executive). It is unfortunate that Beddard’s obituary notice for the Royal Society was written by Sir Peter Chalmers Mitchell, who succeeded Sclater after a bitter, highly political election. In some respects Mitchell was an ideal biographer of Beddard since he had worked in Beddard’s prosectorium and obviously knew him well. However, Mitchell throughout his life seemed hellbent on deriding Sclater and Beddard’s obituary was yet another chance he did not pass over.

Chalmers Mitchell praised Beddard’s working habits in the days of the gentleman scientist:

For a large part of his life he was a harder worker than persons with more ordinary habits could guess. He rose very early, and was usually at his table in the Zoo Prosectorium before 8 a.m. On many days he lunched at the Gardens, taking his notebooks into the restaurant, then worked until 4, when he went home, wrote until an early dinner, again worked after dinner, going to bed at 9. When the routine was broken by his going to a club to lunch, he already had a good morning’s work behind him and could linger in apparent idleness long after the ten-to-four men had ostentatiously hurried away. In later life, naturally, he was easier with himself. 

Beddard did not enjoy a happy life. He married Anne Fletcher in 1886 and had two children but the couple split up. He with the children moved in with his mother in Hampstead. Mitchell continued:

These domestic circumstances are related because they were the first cause of a sense of grievance against life which increased with age, until it became almost a mania of persecution. Apart from the subject of his wrongs, Beddard was a charming companion, with a fund of amusing anecdote that made him a welcome neighbour in clubs or social gatherings. 

It was in his description of Beddard’s work at the Zoo that Mitchell took the opportunity to have a dig at Sclater and remind the world what a great replacement he had been:

During the greater part of Beddard’s tenure of the Prosectorship, there was the unfortunate tradition that the Prosector must always be ready with a paper for the fortnightly Scientific Meetings of the Society. P. L. Sclater, moreover, his official chief, was interested mainly in systematic zoology, and not being an anatomist himself, was over-ready to believe that even a hurried dissection would settle doubtful points in classification. The double pressure led Beddard to produce far too many short papers, and to draw systematic inferences from dissections of single species or even single organs in species. It cannot be said that his output in any part of vertebrate anatomy had a value at all com­mensurate with its bulk. A volume on the ‘Structure and Classification of Birds,’ published in 1895, brought together much useful information ; one on ‘Whales ’ (1900) was pleasantly written; his volume on ‘Mammals in the Cambridge Natural History ’ was a sound and useful compilation. Several others need not be mentioned.


A list of the books he wrote with, in some cases, links to full text sources can be found here.

From Beddards book on animal coloration

Beddard was praised for his work on oligochaetes (which he had done while fulfilling his duties as prosector). Quite how he had time to do this isn’t made clear because he was also lecturer in biology at Guy’s Medical School, as well as external examiner in Oxford and London:

Beddard’s permanent place in Zoology depends on his great ‘Monograph of the Oligochaeta’ (Oxford University Press, 1895) and on the prolonged researches on which it was based. There were already in existence accounts of the group published by F. Vejdovsky in 1884 and L. Vaillant in 1890, but both of these writers had rather neglected the literature on the subject, and subsequent to their volumes very much new information had been obtained by the study of collections from most parts of the world. Beddard had himself dissected and examined nearly all the important types that were known, and had searched the literature carefully. The general account of the anatomy he gave was much in advance of that of any of his predecessors, and his systematic descriptions were clear and well arranged. 

Beddard was elected to the Royal Society in 1892.

The unfortunate taste in the mouth left by Chalmers Mitchell’s account of Beddard’s life—as indeed with much of his writing—extended to reminding the reader, again, of who won the election to succeed Sclater. Beddard, Mitchell wrote, was a candidate but ‘he did not press his claims in face of a general opinion, which he himself frankly shared, that he was not well adapted to the continuous duties of administration of a large organisation’.

Beddard retired from the Zoo, where he was a popular lecturer, in 1915. He died of a heart attack at his house in Hampstead in 1925, aged 67.

Chalmers Mitchell’s comments on the book written by Beddard echo those written by William Plane Pycraft (1868–1942) of the Natural History Museum in an obituary for Nature:

In his books Beddard did himself less than justice. His volume on whales, for example, was good but he could have given us a much better book. The same may be said of his volume on the classification of birds and that on the coloration of animals. In these he seems to have shirked the labour of coming to a decision on the very vexed and controversial points which these two themes presented. He nowhere commits himself to a definite opinion as to whether he does or does not agree with the conclusions arrived at by others, whose views he sets forth without comment. His pages are almost too dispassionate to be helpful.

I looked at the book on animal coloration. I found it an excellent introduction for its time, and surely he should have been praised for presenting different views on ‘controversial points’ without necessarily, in the absence of further evidence or informed knowledge, coming down on one side or the other.

Pycraft (who, remember, was one of those duped by the Piltdown hoax) praised the talks that Chalmers Michell so derided; part of the job of the prosector was to keep the amateur and professionals who gathered for Zoological Society meetings content with their membership:

Those who were privileged to listen to his discourses, at the scientific meetings of the Society, will ever remember his extraordinary facility of expression and the clear and rapid way in which he laid abstruse points before his audience. Few, probably, who were listening had ever made the dissections he was describing, yet so admirable was his presentation of the facts he had gleaned, that they could not fail to grasp the essential points laid before them. He had no rival in this regard.

Beddard’s preserved specimens and descriptions live on. I think Beddard is now best described as an exemplar both of what zoology was all about at the end of the 19th and beginning of the 20th centuries and of the sort of man who worked in the field. And I still rather like, dated as it is,  his mammals book.

Pycraft WP (as WPP). 1925. Dr FE Beddard FRS. Nature 116, 215-216.

Mitchell PC (as PCM).1926. Frank Evers Beddard—1858-1925. Proceedings of the Royal Society B 99, xxxvi-xxxvii.

Sunday, 14 February 2021

HONG KONG: An Urban Wild Boar

AJP was walking to the Aberdeen MTR Station a couple of weeks ago when, much to his surprise, he spotted a wild boar walking along the footpath towards him.

In the 1960s wild boar were very rare, having previously been abundant. So rare that Patricia Marshall in her Wild Mammals of Hong Kong (1967) wrote of ‘there being possibly only one or two families of not more than five individuals in each. One family on Lantau [island], one in the New Territories’.

Now they are said to be everywhere with a massive increase in the past few years. People feeding them are being blamed for their presence in urban areas. This one was the epitome of nonchalance as it sauntered along the street.

It reminds me of the 1934 temperance song:

Yes, the pig got up and slowly walked away

Slowly walked away, slowly walked away

Yes, the pig got up and he turned and winked at me

As he slowly walked away

The genetic history of these pigs would be interesting, especially since there were thought to be none on Hong Kong island (Aberdeen is on the island for those unfamiliar with the place) by the late 1960s. 

Monday, 25 January 2021

Pallas’s Squirrel in Hong Kong: Feral pets, an introduced or reintroduced species…or even a range expansion?

Fifty years ago the sight of a wild squirrel in Hong Kong would have been unthinkable. But now, Pallas’s Squirrel (Callosciurus erythraeus) can be seen both on Hong Kong Island and in the New Territories. I have no reason to doubt the story that these populations were from the accidental or intentional release of squirrels imported for the pet trade. Well…perhaps a nagging doubt.

Pallas's Squirrel photographed in the New Territories of
Hong Kong by AJP, December 2020. Note the black
'spot' near the end of the tail. In the second photograph
the red belly can be glimpsed.

In the 1960s these squirrels, along with Siberian Chipmunks, were being sold as pets in Hong Kong. The ‘lab boys’ had a couple in a tiny cage in their room in the Zoology Department of the University of Hong Kong, for example. In view of the appearance of flocks of feral Yellow-crested Cockatoos we perhaps should not have been too surprised to have seen squirrels in the trees of Government House on our first return to Hong Kong in 1997.

The standard account of these squirrels in Hong Kong is that the ones on Hong Kong Island are different from those in the New Territories. Those on the island are described as belonging to the subspecies C.e. thai, with those in the New Territories as C.e. styani, the former from Thailand; the latter from Northern China. I am not sure how the feral animals in Hong Kong were assigned to these subspecies and having looked up some of the original papers I am even less sure about the identification of thai other than Thailand is perhaps where the animal dealers said they were imported from. The black hairs near the tip of the tail of the ones from the New Territories do, however, fit the description of styani. The import of the Siberian Chipmunk, Eutamias sibiricus, is also compatible with the importation of C.e. styani, into Hong Kong from the same area of northern China.

In many parts of its range the belly of the squirrel, as its specific name implies, is some shade of red. That is true of those in the New Territories of Hong Kong. That was not the case in at least some of those kept as pets. The ones the lab boys kept were a light yellowish grey—as were those we saw in the gardens of Government House 30 years later.

It does seem odd that a native squirrel had never been reported for Hong Kong. The question is if they were once there and had been extirpated or had never even been part of the native fauna. Two squirrels apparently from near Canton (now Guangzhou)—only 135 km (85 miles) from Hong Kong—were collected by John Reeves between 1812 and 1831; the skins are in the Natural History Museum in London. They are currently assigned to a subspecies, C.e. castaneoventris, with a distribution south of the Pearl River including the island of Hainan. Nothing seems to be known in formal descriptive terms of the Pallas’s Squirrels that occur over much of China (including the mainland north of the Pearl River adjacent to Hong Kong) and this leads me to the first of my nagging questions: is it just possible that the squirrels in the New Territories of Hong Kong are not feral but are native squirrels that have come over the border as Hong Kong became reforested after the devastation of the hillsides for firewood during and shortly after the Japanese occupation?

The whole taxonomy of squirrels of the genus Callosciurus seems to this outsider as a mess, in part due simply to a lack of series of specimens from most parts of the range. Clarity has not be advanced by simplistic molecular phylogenetic studies (using only mitochondrial DNA). That leaves me with a second nagging question: why, if two apparent subspecies were imported for the pet trade in the 1960s has one become feral in mainland Hong Kong and the other on Hong Kong Island? Surely, both would have been sold in the pet shops and bird markets on both sides of the harbour. Did they interbreed on the mainline side and if so does that mean that the ‘styani’ coloration is dominant to the ‘thai’?

Tackling the questions on the origins of the Pallas’s Squirrels would also help settle the obvious corollary: can those in Hong Kong be classified as an ‘introduction’ or a ‘re-introduction’ or even a natural range expansion?

Lurz PWW, Hayssen V, Geissler K, Bertolino S. 2013. Callosciurus erythraeus (Rodentia: Sciuridae). Mammalian Species 45, 60-74.

Moore JC, Tate GHH. 1965. A study of the diurnal squirrels, Sciurinae, of the Indian and Indochinese subregions. Fieldiana 48. Chicago: Chicago Natural History Museum.

Tuesday, 12 January 2021

A Hong Kong Moth

 AJP found this moth in Hong Kong last week. It seems to be a female Eudocima homaena, noted as being a pest on orange trees in parts of its range.

Monday, 11 January 2021

Do any introduced Painted Frogs still survive in Manchester?

Discoglossus pictus from Sicily
Fabrizio Li Vigni here
In my last post I described how Louis Lantz had bred Painted Frogs (Discoglossus sp.) in Manchester. Because he was unable to rear the young to adulthood he released them into his garden. There grew and bred, and he described how he could then collect them for breeding experiments and to pass on.

The frogs left to fend for themselves in the garden spawned in small open air ponds and spread in neighbouring gardens and garden ponds. This introduction was noted in Deryk Frazer’s Reptiles and Amphibians in Britain (Collins, 1983) with the comment that it was not known whether there were still individuals surviving from Lantz’s releases.

No address was given for Lantz in the 1947 paper in which he discussed his keeping and breeding these frogs and so I suspect that anybody searching the Manchester area would have had no clue as to where to begin looking. The 2017 biographies of Lantz provide two addresses in  the Manchester area where he kept and bred amphibians and reptiles. With the help of genealogy search sites it is possible to pin down the approximate dates he was living at the two locations.

The paper published in 1947 was submitted in March 1946. Given the usual period taken to prepare a final draft we can estimate that Lantz wrote his part at the end of 1945 or in very early 1946. He wrote that he had made the observations ‘during the last 15 years’; in other words around 1930. The first breeding experiments he described were in 1932. At this time Lantz was living at 9 Waterpark Road, Manchester 7. I see from Google Earth that there is a lake in Broughton Park only 130 metres from Lantz’s house. He was still there with his family in 1935. Unfortunately at the time of the 1939 Register, a special census taken in preparation for war, he and his wife were guests at a hotel in Wales but by 1940 he had moved to 2 Kinnaird Road at Withington where the photograph I showed in the last post of his greenhouse was taken. It was at Kinnaird Road that Lantz collected spawn from a neighbour’s pond.

In recent years the single species of Painted Frog has been split into five or six. Lantz explained where he had obtained his frogs and it therefore possible to assign currently recognised species [in square brackets below] to the ones he collected, bought or was given:

Some of the material was collected by the author on Port-Cros and Levant Islands near Hyeres, where the species had not previously been recorded [D. sardus], and later also on Corsica [D. sardus but also possibly D. montalentii]. A few Sardinian [D. sardus] and Portuguese [D. galganoi] specimens were obtained from dealers, but many fine and valuable animals are due to the kindness of Mr J. Armitage (1 specimen from Corsica [D.sardus or D. montalentii]), Gen. M. Berquet (10 specimens from Tunisia [D. pictus]), Mr O. Cyren (3 specimens from Morocco [D. scovazzi]), and Mr R. Maxwell Savage (7 specimens from Port-Cros [D. sardus]), to whom sincerest thanks are expressed. 

In respect of Lantz’s breeding experiments between what were clearly D. sardus (then considered a subspecies, D. pictus sardus) from Sardinia and Port-Cros and D. pictus ( D. p. pictus) from Tunisia, it is interesting to note that these two ‘species’ interbred and back-crossed freely. As in his studies on newts he was interested in the inheritance of skin colour and pattern. What was then pictus came in two dorsal patterns: spotted and striped; sardus spotted only. He found inheritance was of the simple Mendelian type, with ‘striped’ dominant over ‘spotted’.

However, the purpose of this post was not to question whether the current species recognised are good ‘biological’ species, but to point out the existence in the 1930s and 1940s of breeding sites in the Manchester area of introduced Painted Frogs. Although the odds of their continued existence seem long, it is surprising how many gardens in England still have thriving colonies of introduced Midwife Toads. Lantz was not the only herpetologist to introduce deliberately or accidentally Painted Frogs in England. North London in 1960 was the second instance noted by Frazer. Painted Frogs were also commonly imported by dealers, particularly in the earlier decades of the 20th century and numbers must have been released into insecure ponds and vivaria over the years. There are also at present current breeders of one or more species of Discoglossus in Britain.

But back to the original question: has anybody in Manchester had a look or plans to look for Painted Frogs? 

Lantz's plate from the 1947 paper showing his breeding experiment
Original capton wording superimposed on each figure

Distribution of Painted Frogs (Discoglossus)

Bruce HM, Parkes, AS, Lantz LA. 1947. Observations on Discoglossus pictus Otth. Proceedings of the Royal Society B 134, 37-56 (plus two plates).