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.

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.

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).

 

Louis Lantz: Frenchman, Manchester resident, outstanding herpetologist, and important in wider biological circles in 20th century Britain

My first memory of seeing the name Louis Lantz is of being mystified by the appearance in Malcolm Smith’s book, The British Amphibians and Reptiles I had taken out from the local library, of a graph showing growth curves after metamorphosis for three hybrid newts. That graph accompanied the text: ‘Mr L.A. Lantz’s observations on growth shew that the rate depends largely on the quantity of food available and on the length of period during which, because of low temperature or low humidity, little or no food is taken’. I remember being intrigued—who was this Mr Lantz and why did he have hybrids between two species, Triturus cristatus and Triturus marmoratus?*

Only many years later did I begin to learn who Lantz was, why he worked in Manchester, and of his various contributions to herpetology. Biographies published in 2017 in French and In English have attempted to make Lantz and his classical herpetology better known in his native France and in Russia where he had worked. Unfortunately his biographers have largely omitted or underestimated his rôle in the British scientific scene and in the development of genetics and cytogenetics by some of the big players in this then burgeoning field.

Lantz has been described as an amateur herpetologist. That he was in the sense that he was not paid for working on amphibians and reptiles. But he was a professional scientist and technologist who worked in herpetology in his spare time. Lantz was a scientist whether involved in his profession or his ‘professional’ hobby which is why he found collaboration with the major figures in genetics a normal part of scientific discourse. He is also described as having ‘kept salamanders as pets’. I think those of us who have or still do keep reptiles and amphibians would object strongly to use of the word ‘pet’ in such a context.

Louis Amédée Lantz was born in 1886 in Mulhouse, Alsace, now part of northern France but then annexed to Germany. After studying zoology and botany at the University of Montpelier in 1903-4 he moved to the school of industrial chemistry in Mulhouse. There be obtained a diploma in chemical engineering. The school specialised in teaching the use of dyes for the important local textile industry which concentrated on printed fabrics. The school attracted a number of Russian students and Lantz found a job in Russia in 1907. From 1908 he specialised in cotton dyeing and printing at a vast factory in Moscow. Forced to leave in 1918 because of the Russian Revolution—and having married a Russian—he held various jobs in France. Then in 1923 he was appointed Director of Research at the Calico Printers’ Association in Manchester. He stayed there until his retirement in 1951 at the retirement age of 65. Partly, he recorded, because of his wife’s health, he returned to France, intending to live in Paris in order to work at the natural history museum. He died in Lucern, Switzerland in February 1953.

From Ineich et al 2017

   

The laboratory in Manchester, was, for its time, a big one. It employed 20 graduates and 40 technicians seeking to improve and to develop new techniques for printing and dyeing. At the time of formation of the company by merger, Calico Printers was producing 80% of Britain’s output of printed cloth. As well as printing and dyeing, Lantz was also responsible for the development of new, synthetic fibres and coatings. Terylene or PET, later manufactured by ICI, was one outcome in 1941. He and his team had numerous patents for processes and materials they invented.

Having started to keep reptiles and amphibians at home in Alsace, Lantz took every opportunity to study reptiles in the wild, in the Caucasus while he was working in Russia, for example, and to undertake breeding experiments that directly addressed questions in systematics and taxonomy of the time. For example, were some European lizards simply geographical variants (subspecies) or true species? He thus became interested in the whole question of species definition and of genetic reproductive barriers between them. That is why he tried to breed hybrids in captivity and then see if their offspring were fertile.

He came under the influence of the German herpetologist Wilhelm Georg Wolterstorff (1864–1943), a major player in promoting amateur herpetology through the keeping of live animals and in linking amateurs with professional museum scientists, particularly in German-speaking countries. Wolterstorff was particularly interested in newts and salamanders and realised the value of hybridisation experiments. In 1903 he reported that a long-recognised species of newt, Triturus blasii, from western France was in fact a naturally-occurring hybrid between male Great Crested or Warty Newt, Triturus cristatus, and female Marbled Newt, T. marmoratus. Lantz took up the challenge of breeding such hybrids in order to investigate what was going on in terms of genetics in the zone where the northern T. cristatus and the southern T. marmoratus overlap and in which hybridisation sometimes occurs.

I will not describe further Lantz’s work on the lizards of the Caucasus, much of it done in collaboration with the Swede and fellow chemical engineer, Otto Cyrén (1878-1946) and which continued after he left Moscow in 1918. That and other aspects of his work, including keeping and breeding the Common Chameleon (Chamaeleo chamaeleon), have been extensively covered in the 2017 biographies. I shall instead, add to that information by indicating his involvement with the highest levels of research in genetics and cytogenetics in Britain.

A clue to the importance placed on Lantz’s work with newts can be found in the following quotation:

A few people have the capacity for noticing the exceptional very highly developed. I think particularly of my late friend L. A. Lantz, who was secretary of the British Colour Council. This is not, as might be thought, concerned with the rights of immigrants from tropical countries but with textile dyes; and its secretary doubtless had a fine eye for colour differences. He also had a fine eye for lizards and newts. His most remark­ able achievement in this respect was perhaps noticing that he could not tell the sex of a lizard which he saw running about, catching and killing it, and finding that it was an intersex. 

This is from an essay, On Expecting the Unexpected, published in the Rationalist Annual in 1960 and included in the collection, Science and Life, published as a book in 1968. It was written by J.B.S. Haldane. As I said, the top level of evolutionary genetics at the time. But Haldane (and his second wife, Helen Spurway (Haldan [sic] in the 2017 biography in English) was not the only Fellow or future Fellow of the Royal Society that Lantz was supplying with animals and collaborating with. He worked with Michael James Denham White (1910-1983, FRS 1961) then at University College, London, and more significantly with Harold Garnet ‘Mick’ Callan (1917-1993, FRS 1963) on the cytogenetics of his hybrid newts. Newts have large chromosomes and are particularly suitable for studying meiosis; the number of chiasmata between pairs can more easily be counted. After Lantz’s death, Callan and Spurway continued their collaborative work on meiosis in hybrids between different geographical ‘races’ of Triturus cristatus. I have written elsewhere about the people Haldane recruited in the late 1940s to work with Helen at University College London in breeding newts (and fish). The story can be found here. 

Not apparent from the biographies was the many years needed for Lantz’s cross-breeding experiments. From an initial breeding in 1944—in wartime Manchester where Lantz was, as Haldane noted, appointed by de Gaulle as representative of the Free French Forces—the young newts only reached maturity in 1947 and those from back crosses made in that year in 1949-50. Fruit-flies, with a generation time of 1-2 weeks, they were not.

Interest in what determines the skin colour and pattern in amphibians was high in the first half of the 20th century. Paul Kammerer—another protégé of Wolterstorff—had claimed, certainly erroneously and probably fraudulently, that the pattern of stripes and spots on salamanders was determined by the environment. The examples he provided were soon shown to be of salamanders from different parts of the geographical range and that the major differences were genetic in origin. The physiological, i.e. short-term, mechanisms that cause a frog to change colour when moved, say, to a pale substrate, were also becoming clear. Lantz set out to determine what effect a light or dark background would have on larval salamanders and whether changes in colour or pattern were carried into adulthood. He began this work in 1938 on Triturus cristatus. His paper was published posthumously in Haldane’s journal, Journal of Genetics in 1953†.

Lantz also showed that other claims of Kammerer’s, oviparity in viviparous lizards and ovoviviparity in salamanders, were part of the normal plasticity of the species involved in different parts of their geographical range and not novel, acquired, heritable traits.

It was not only his success with newts that attracted attention. He was also breeding the Painted Frog, Discoglossus pictus, at home in Manchester. Alan (Sir Alan from 1968) Parkes (1900-1990, FRS 1933) and Hilda Bruce (1903-1974) (of the famous Bruce Effect in mice) of the National Institute of Medical Research got to know of this and were keen to explore the potential of a species which breeds spontaneously in the summer or can be induced to breed in the winter under laboratory conditions. Lantz supplied them with frogs and he wrote a note as an annex to their paper which described how the adults and tadpoles were kept and bred. Neither Lantz nor Bruce and Parkes succeeded in rearing the metamorphosed young. This problem, common at the time, was almost certainly attributable to deficiencies of calcium and Vitamin D. Lantz did though release young into his garden where they thrived and spread into neighbouring gardens.

Also in touch with Lantz was C.H. Waddington (1905-1975, FRS 1947) who had earlier used Discoglossus pictus for pioneering work in developmental biology. Waddington, then in Edinburgh, was taking Lantz’s advice on breeding the frogs in 1951.

Lantz did not abandon his classical herpetology nor his keeping and breeding of many different species of lizards and amphibians while in Manchester. Far from it. He collected in the Mediterranean region and the Pyrenees. He was clearly in close contact with H. W. Parker (1897-1968) at the Natural History Museum in London; some of his specimens are in the collection.

Thus, while emphasis has been on Lantz’s contributions to classical ‘museum’ herpetology, he was a more significant figure in British science.  Capitalising on his lifelong interest and success in keeping and breeding reptiles and, particularly, amphibians in captivity, he had an important enabling rôle in the research of leading British scientists working on evolutionary genetics and cytogenetics in the mid-20th century.

Louis Lantz was described by Parker in a short obituary for the journal Copeia as one of the outstanding figures in herpetology. I agree.

*There is an error in the text in that the animals are referred to as T. cristatus marmoratus rather than T. cristatus x marmoratus. Smith ought really to have said that he was showing the best available data to make his point on growth rate and the fact they were interspecific hybrids was not germane.

†The results were clear. White or black background (on which the larvae turned lighter or darker respectively) had no effect on the dorsal spot pattern after metamorphosis but the lightness or darkness of the ground colour could be changed with a change in background. For ventral coloration, the results were different. A white background suppressed while a black background promoted the development of black markings. The ventral coloration and patterning could not be reversed by changing the background in adults.

A list of Lantz’s publications is included in the 2017 biographies. However, because there seems to have been confusion when a publication in Proceedings of the Royal Society was listed and scanned for online viewing, a note of his appended to but part of a full paper has been shown as a separate publication. The correct reference is:

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

These are the two biographies I refer to in the text. The shorter and earlier one is:

Anon. 2007. Lantz, Louis A. (1886-1953). In Contributions to the History of Herpetology Volume 2, edited by Kraig Adler, p 139. Society for the Study of Amphibians and Reptiles.

The 2017 biography has been published twice, once in the USA in English and in a slightly longer form (with an additional author) in France in French:

Ineich I, Doronin I. 2017. Louis Amédée Lantz (1886-1953): The Life and Work of an Alsatian Pioneer of European Herpetology. Herpetological Review 48, 93–108. 

Ineich I, Doronin I, Lescure J. 2017 Vie et œuvre de l’Alsacien Louis Amédée Lantz (1886-1953), pionnier de l’herpétologie européenne. Bull Soc Herp Fr (Bulletin, Société herpétologique de France) 162, 55-106.

Beavers in Britain. Estate beavers in the 19th and 20th centuries

Successful attempts to reintroduce the Eurasian Beaver to Britain are now well known. Fortunately, and despite opposition, the various releases both ‘legal’ and ‘illegal’ (how it can be illegal to release animals native to mainland Britain I have difficulty fathoming out) seem to be working. Beavers are said to have been extirpated in the 1500s by hunting for fur, meat and castoreum, a secretion formed apparently by the walls of the castor sac near the anus, which was used in perfumery and as a food flavouring.

Articles have reported historical accounts of beavers being kept on large estates, possibly with a view to their eventual wider release. Most articles report that the beavers involved were not the native Eurasian Beaver (Castor fiber) but the North American species, Castor canadensis. However, examination of original records indicated that this was not so in one of the introductions, the first I describe.

The 3rd Marquess of Bute, John Patrick Crichton-Stuart (1847-1900), acquired beavers for his estate Mount Stuart on Bute, an island in the Firth of Clyde thirty miles from where I am writing this article. He is said to have imported four beavers in 1874 to be kept enclosed in a small wood. Since animals in zoos and other collections never ‘die’ but are ‘lost’, ‘poor doers’ and the like, these beavers were ‘not succeeding’  A further seven were then obtained in 1875. Those animals bred but the total numbers at any one time seemed to vary with the person doing the reporting if not the counting; 12 to 28 seems to be the range. As I indicated, most second-hand reports of the beavers on Bute have stated that they were Castor canadensis. However, the excellent website of the Bute Museum website contains more accurate information: 

Beaver Castor fiber were introduced to Bute in 1874 by the 3rd Marquess of Bute, but the species had died out by 1890. They were at one time reported to be the North American Beaver Castor canadensis, but correspondence in the Bute Archives revealed that the Beavers came from Scandinavia [references to research by the late Dr Jack Gibson].

Another group of beavers was in the south of England and they were reported as Castor canadensis. An account (Beavers in Sussex!) was given by L.R. Brightwell* in Animal and Zoo Magazine in 1938. Sir Edmund Loder (1849-1920) the then owner of Leonardslee, an estate near Horsham in West Sussex, at one time kept coypu and capybaras as well as the beavers. Brightwell’s seems to be the most accurate account of the date of their acquisition—around 1897. However, a letter to Nature in 1897 stated they had been there since 1889--the date Loder bought Leonardslee from his in-laws. A letter to The Times in  2010 stated that according to an old magazine article the beavers had been obtained by Loder’s great-grandfather in the 1850s. However, that cannot be the case because Loder did not buy the estate until 1889. According to the website for Leonardslee Gardens, beavers were on the estate until 1947.

Brightwell visited Leonardslee, where he was shown around by a George Stoner†, and described the ‘beaver yard’:

This is a lake, a quarter-mile long by fifty yards wide, hemmed in by trees and an inconspicuous barrier of sheet iron planted a yard deep in the soil. Such trees that stand within the enclosure wear skirts of sheet iron, and the necessity of such safeguarding is at once apparent. The dead lie all around—sixty-foot pine, larch and beech, white as ivory, for not one particle of bark has the beaver left upon them.

An early disaster came with flooding after a storm. The beavers swam over the barrier and reached the sea, thirteen miles down stream. There some fishermen in a boat hit the strange animals over the head and carried the corpses ashore in order to find out what they were.

A heavy iron grid spanned the stream from the lake. Every night the beavers attempted to build a dam at that point and every morning the estate worker with the job of looking after the beavers had the job of undoing their labours in order to prevent flooding. 

As well as beavers, both the Marquess of Bute and Sir Edmund Loder, acquired wallabies for their estates; those at Leonardslee are still there. The ones on Bute were released into the wild but I do not know how long they survived there.

For some time it seems the two species of beaver, North American and Eurasian were regarded as one. But they are ‘good’, true biological species, with different numbers of chromosomes. Attempts at hybridisation have failed to produce live young and where introduced C. canadensis meet C. fiber in Europe there has been no breeding between the two.

Brightwell remarked in discussing the tail of the beaver its use to generate an alarm:

Used as an alarm gun, it can strike the water with a force like a pistol shot…

That sound, which made me jump, was my first introduction to Castor canadensis. In 1973 and up very early because I couldn’t sleep on with 5-hour jet lag I wandered around the campus of Colby (now Colby-Sawyer) College in New London, New Hampshire, just after dawn. I stopped to look at chipmunks in the woods and as I passed the pond, the ‘force like a pistol shot’ hit my ears. I turned and there was a beaver. I watched the beavers there for several mornings that week and again when I was there later in the 1970s for Gordon Conferences; I was even able to show Americans their first beaver. However, by the 1980s I did not see any and the latest view on Google Earth shows the pond largely hemmed in by a new car park.

*Leonard Robert Brightwell (1889-1962) was a well-known and prolific author and illustrator. He had strong academic zoological connexions since he illustrated The Science of Life for the authors, H.G. Wells, Julian Huxley and G.P. Wells.

†I find George Allen Stoner (1869-1964) living in Horsham, three miles from Leonardslee, described as an ‘estate worker’ in the 1939 Register.

Rain Stimulates Many Frogs to Breed. But HOW does it work?

Smilisca baudinii from Central America

In my last post here I remarked on the lack of knowledge of how the onset of seasonal rain induces breeding in a number of tropical birds. We know why that happens: the onset of rain presages the explosion of insect life on which young birds are fed but we do not know how that stimulus works.

Amphibians also breed in response to rain and some of them ought to provide an opportunity to discover what it is about rain that signals to the brain and sets in train the neuro-hormonal events that lead to breeding behaviour, egg production and fertilization.

I should make a distinction here between a physiological state of readiness to breed and the actual trigger that sends a signal loud and clear to ‘go’ such that in a matter of hours eggs have been laid and fertilized. It is this latter effect of rainfall I am discussing.

Many tropical frogs can and do breed throughout the year but only do so after rain. Herpetologists make use of this phenomenon to induce breeding in captivity. All sorts of devices have been rigged in the past to mimic the whole manifestation of a tropical downpour: simulated rain; tape recordings of heavy rain and thunder; setting off the simulated shower during a period of decreasing barometric pressure etc. Sometimes such manipulations work; sometimes they do not. When they do work though the results are spectacular; within hours there are masses of frogspawn.

Such set ups in captivity ought to enable the identification of what it is about rain that is important and to determine the senses that are being activated to pass on that signal to the brain. Thirty-five years after I was either breeding or attempting to breed treefrogs from central and northern South America, the use of a ‘rain chamber’ is established practice for some species, like the Red-eyed Tree Frog (Agalychnis callidryas). At this stage I should point out that a rain chamber is a vivarium arranged with a pump to recirculate water through a spray head such that ‘rain’ falls onto the plants and inhabitants below. It should, therefore, be possible to devise experiments to test the factors that might be important. For example, there have been suggestions that a sharp rise in humidity is a sufficient stimulus - easily tested by having a netting divider across the vivarium with frogs but not ‘rain’ on both sides; sealing the vivarium would enable changes in barometric pressure to be tested.

Red-eyed Treefrog from Central America

The outcome of such experiments might have a bearing on the old problem of how frogs and toads find their way to ponds in spring. A famous but now largely forgotten British scientist, Ronald Maxwell Savage (1900-1985) whose ‘professional’ hobby was studying the Common Frog, Rana temporaria, obtained some evidence that frogs can smell the algae growing in fresh water and thus move towards the source of the aroma. Could chemical sensing be involved in tropical frogs? Do they respond more reliably to recirculated aged vivarium water or to fresh rain water at the same temperature? How important is change in temperature? The possibilities seem endless but some pretty simple experiments would I am sure soon uncover which factors could be discounted at least in one species. We do not, of course, know whether the key factor about rain that stimulates breeding is the same in tropical tree frogs as in, say, a desert frog in Africa or Australia.

I was not able to take my breeding of species thought to be susceptible to tropical rain very far for the simple reason that other species I had, particularly dendrobatid or poison-dart frogs, were breeding so well that rearing their young was taking all my spare time. However, one species that sometimes did and sometimes did not respond to an artificial tropical storm was Smilisca baudinii, which has a number of common names including Mexican Treefrog and Masked Treefrog. One spawning by several females goes a long way and I raised a hundred or so past metamorphosis to a size where they could be passed on to others. With those which did not breed after an artificial downpour, an injection of human chorionic gonadotrophin (i.e. as in the human pregnancy test using Xenopus) resulted in fertilized eggs the next day. In other words the frogs had been ready to breed but my ‘rain’ had not been a sufficient or only stimulus.

Given the importance of rain in stimulating breeding in some amphibians as well as in some birds and other organisms, surely it is time we had experimental evidence on what it is doing and how it works.

Smilisca baudinii - captive-bred juvenile

Rain and seasonal breeding. An unsolved problem in physiology

Red-billed Quelea - male in breeding plumage
Bernard DUPONT from FRANCE, CC BY-SA 2.0
<https://creativecommons.org/licenses/by-sa/2.0>
via Wikimedia Commons

Background

The origins of this story—and its unanswered questions—go back to the 1930s. J.R. Baker (1900-1984) was working at Oxford in the 1920s on the control of sperm formation in crickets when he went on the first of several expeditions to the New Hebrides. There, amongst other observations, on the large proportion of intersex domestic pigs, for example, he began to ask the question of what controlled the seasonality of reproduction of birds and mammals—and plants—in the tropics where there may be little or no variation in the environment during the year. He therefore planned another expedition to Espiritu Santo, the largest island of the New Hebrides, now Vanuatu. To continue the work after other members of the expedition had to return to Oxford, he took Tom Harrisson and, in Sydney, recruited ‘Jock’ Marshall (1911-1967). Other members of the expedition were his first wife, Inezita*, his sister Geraldine and Terence F. Bird (about whom I have no further information).

I will not dwell on the relationship between Baker and Marshall here. It is well described in the notes edited by Marshall’s late widow, Jane, here. In short, it began very well but in later years deteriorated badly. Nevertheless it was Baker and Marshall whose names became associated with factors controlling seasonal breeding in the tropics and of putting the questions in an evolutionary framework.

At first glance Baker and Marshall made an unlikely combination. Indeed, I knew people who worked in Oxford being surprised that Baker, the quintessential don, had ever ventured to the tropics or had qualified for a pilot’s licence. But he was the great-nephew of Sir Samuel Baker, the explorer of the Nile and Central Africa. Marshall, only later to obtain a degree at Sydney and an Oxford D. Phil. with Baker was a self-confessed larrikin, still sorting himself out after shooting off his arm in an accident but helping at the museum in Sydney and going on long birding trips to various parts of Australia. They were, along with Mrs Baker, Terence Bird and Harrisson, as tough as old boots. And they needed to be for the conditions encountered on Espiritu Santo were rough. This is how Jane Marshall describes just part of it:

There is constant talk in both their diaries [Marshall and Harrisson] of each others sores and fevers, dysentery and leprosy among the natives, malaria and one of the government men with blackwater fever for the third time. Jock talked of jagged coral disguised in foliage always ready to gouge a new wound, blowflies that deposited maggots on their blankets which then entered their open flesh, mosquitos, ants, spiders, cockroaches so numerous they scuttled round their feet nibbling at toe-nails while they were eating; 'they flew from wall to wall, gradually reducing calendars, photographs and record papers to flimsy ribbons; they ate holes in the bellows of my camera and shaved the titles from our books.' It was no tropic idyll; a body-wearing, tearing climate; 'each day at meal times Tom and I sat with our scarred legs in kerosene buckets of lysol and hot water - and we did much of our work in the kerosene tins each evening closely examining the lesions and jealously regarding each other's progress.' 

The expedition made detailed meteorological records as well as studying the reproductive organs of a number of animals and plants 'in an endeavour to determine the existence, periodicity and proximate causes of breeding seasons in one of the most uniform climates in the world.'

Baker drew together his survey of breeding seasons, including data from Espiritu Santo, in a chapter, The Evolution of Breeding Seasons, for a book to celebrate the 70th birthday of E.S. Goodrich published in 1938. On the wet tropics he wrote:

Occasional species may breed all the year round in certain places…but the general rule is for birds to have breeding seasons. The Oxford University Expedition to the New Hebrides…was struck by the seasonal behaviour of organisms in a little-changing climate. The climax was presented by the insectivorous bat, Miniopterus australis, the adult females of which all become pregnant once a year about the beginning of September, despite the constancy of climate and the fact that they hang all day in a dark and almost thermostatic cave.

Although the results of the expedition demonstrated seasonality of breeding in the wet tropics, ‘Baker and his colleagues were unable to show in the New Hebrides what factor or factors determined its onset, e.g. food supplies for the offspring, or more direct environmental factors such as rainfall, day length, light, etc.’

To a great extent the work of Baker and Marshall on what happens in the tropics was overshadowed by research, begun by William Rowan (1891-1957) in Canada, which showed that seasonal change in daylength is the major factor controlling the onset of breeding in organisms that live nearer the poles. Not only was that phenomenon demonstrated but the neuro-hormonal pathways that control the seasonal growth and activity of the reproductive organs by that route could be, and were, worked out. There have also been suggestions that even relatively close to the equator daylength is actually important in some birds. At latitudes of up to 10° the variation throughout the year is less than 1 hour of daylight per day.

Baker largely moved on to cytology and its techniques, a number of which he had applied to the reproductive organs. The torch for studying the factors controlling seasonal breeding in birds in the tropics was carried by Marshall until his death in 1967. His general thesis was summed up by the late Brian Lofts in Marshall’s obituary:

He strongly believed that the seasonal reproductive cycles of most birds were based on an autonomous cycle synchronized by a spectrum of environmental stimuli. These he classified into either accelerators or inhibitors. He always stressed that there was no single universal environmental regulator and that different species had evolved a response to different environmental stimuli.

What those environmental stimuli are and how they work bring me to the reason for writing this article.

Rainfall

In his 1938 chapter Baker, after scouring the literature of naturalists, described a whole range of environments in which the onset of rain after a dry season, or, in some cases longer drought, was associated with the onset of breeding in birds, amphibians and reptiles. Many of these observations are now of course well known. For example:

The tendency of tropical African birds to breed whenever the rains start has been remarked by several naturalists, and it has been pointed out that those species which breed in the spring in the subtropical parts do so in the tropical regions whenever the rainy season happens to be.

It was Marshall who demonstrated experimentally ‘the importance of rainfall as a breeding “timer” in an equatorial species’. That species is Quelea quelea, the Red-billed Weaver or Dioch, the most numerous non-domesticated species of bird on earth. I have never seen a large flock of the size justifying the bird’s description as ‘Africa’s flying locust’ because of its devastating effect on seed crops. We have however, seen impressively large flocks flying to roost before dusk against the backdrop of spray clouds from the Victoria Falls, from the verandah of the eponymous hotel on the Zimbabwean side of the Zambezi. And yes, a glass was raised to Jock Marshall; indeed some of the flocks were seen through the bottom of a glass.

However, despite a continuing appearance of paper after paper discussing the effects of rainfall on the onset of breeding of birds and how that stimulus might be more or less important than, say, changes in temperature or some other environmental factor, nobody so far as I am aware, answered the question of how rainfall brings about the hormonal stimulus to the reproductive system. Baker signalled the importance of the mechanism or mechanisms involved noting:

The receptor whose stimulation causes certain animals to breed when it rains is unknown, nor is it clear whether the stimulant is the rain itself or the small saturation deficit of the atmosphere or the existence of ponds or floods. It has been suggested in the Cape Verde Islands it is the green vegetation resulting from the rain, rather than the rain itself…

All sorts of possibilities of what it is about rain that is physiologically important. Sight, smell (of wet earth for example), touch, atmospheric pressure, change in temperature…and so on The list of possibles seems endless. But it cannot be beyond the wit of man to devise experiments to find out. Even more observational studies that produce associations will not suffice; experiments are needed. 

In this article, I have confined myself to mainly to birds since that was the main interest of Baker and Marshall. In a follow-up I will deal with amphibians since there is the possibility of a more convenient experimental approach to determining how rainfall stimulates breeding.

There may, of course, not be a single mechanism by which rainfall stimulates breeding even within a species, let alone between different species. But, more than 80 years since Baker wrote his chapter, it does seem remarkable that we still do not know the answer.

*Her affair with Richard Crossman, (1907-74), the future Labour MP and Minister caused a great scandal in Oxford. He is referred to tangentially in Baker’s Biographical Memoir: ‘Inezita Hilda having been captivated by the charm of the Vice-Warden of New College’. They married in 1937; she died in 1952.

Baker JR. 1938. The evolution of breeding systems. In, Evolution, edited by G.R. de Beer. Oxford: Clarendon Press.

Lofts, B. 1968. Professor Alan John Marshall, D.Sc., D. Phil., 1911-1967. Ibis 110, 206-207.

Willmer, E.N., Brunet, P.C.J. 1985. John Randal Baker. 23 October 1900-8 June 1984. Biographical Memoirs of Fellows of the Royal Society 31, 33-63