Salt glands in extinct marine reptilian killing machines

A time traveller in  the late Jurassic and early Cretaceous, around 150 million years ago, would be wise to avoid the open sea, for there she would have encountered reptilian killing machines, thalattosuchians. These reptiles were 4-5 metres in length and belonged—just like modern crocodiles—to the Crocodylomorpha, a once diverse group of animals.

Palaeontologists have established the thalattosuchians had morphological features that can be linked to living in pelagic or oceanic environments. I will not dwell on those adaptations but concentrate on one which has been the subject of a recent paper from Argentina concerning a new specimen of Dakosaurus andiniensis.

When we wrote our monograph on salt glands in 1975, there had been no search for evidence of their presence in extinct reptiles. However, it seemed highly likely that they must have been there. As a result of what we wrote, in the late 1970s I had a very enjoyable day with the late Peter Whybrow (1942-2004) at the Natural History Museum in London. He wondered whether the obvious depressions in the skull of hadrosaurs—duck-billed dinosaurs—could have been salt glands. Although semi-aquatic herbivores, there was the possibility they could have been potassium secreting glands as in the Common Iguana of South America. We also took the opportunity to look at a range of extinct marine reptiles, including ones collected by Mary Anning, and I was able to see clear depressions in the skull indicative of the presence of nasal salt glands.

In recent years there has been considerable interest in the presence of salt glands in dinosaurs and their relation to the morphological adaptations associated with a presumed marine or brackish water habitat.

In Dakosaurus andiniensis the arrangement of the internal anatomy is such that the nasal glands drain through a ‘nostril’ on either side of the snout via the antorbital sinus. However, a new twist in the story was discovered—a rearward extension of the antorbital sinus to form a suborbital diverticulum. That diverticulum is interleaved between the muscles that operate the jaw. Therefore, it was argued, operation of those muscles could be used to compress the diverticulum and expel rapidly secretion from the nasal salt glands gathered there. An analogous clearing of the salt glands can be seen and heard in the Galapagos Marine Iguana which snorts to cast the concentrated salt solution from its nostrils to the four winds.

What seems to be unknown is their mode of reproduction. From the little I have read, crocodylomorphs were oviparous, with aquatic forms having to lay their eggs on land. If so then a mechanism to expel actively secretion from the salt glands makes sense in that it would prevent salt encrustation and potential blockage of the system caused by evaporation.

These and related studies on the thalattosuchians appear to show an evolutionary trend from forms that lived in fresh water to those completely at home in a fully marine environment. They are also interesting in that modern crocodilians, the only survivors of the crocodylomorphs, have no sign of a nasal salt gland. Instead, the Estuarine crocodile or Saltie to Australians, was found, thanks to the efforts of Gordon Grigg at the University of Queensland, to have salt glands in its tongue.

The authors of the paper on Dakosaurus andiniensis, from the Universidad Nacional de La Plata, make the point that the presence of what must be salt glands in their specimen suggests that the animals could have dealt with a variety of prey from fish (usually, I see, described as the prey), other reptiles, all of which would be relatively low in salt, to invertebrates like squid which have the osmotic concentration of salt water. A specimen of a species of thalattosuchian was discovered in Cambridgeshire with stomach contents that included cephalopod hooklets, fragment of belemnite rostrum and bones, possibly from a pterosaur, suggesting these animals eat anything they can get hold of. I wonder if somebody would like to sit down and calculate the likely weight of the salt glands of Dakosaurus or other thalattosuchians as a percentage of their body weight and then do some armchair physiology, taking known secretory rates of salt glands and food intake for a reptile of that size, in order to calculate whether the salt glands could have coped with a mainly vertebrate diet or one containing lots of osmoconforming invertebrates like squid and other cephalopods. The results would be interesting either way. In other words, we could indulge in physiological time travel.

Young, Brusatte, De Andrade, Desojo, Beatty, Steel, Fernández,
Sakamoto, Ruiz-Omeñaca, Schoch. 2012.
PLoS ONE, 7, e44985, doi:10.1371/journal.pone.0044985

Fernandez MS, Herrera Y. 2021. Active airflow of the paranasal sinuses in extinct crocodyliforms: Evidence from a natural cast of the thalattosuchian Dakosaurus andiniensis. Anatomical Record, 1–16. https:// doi.org/10.1002/ar.24678 

Tinned fish for the Australian Army canned; zoology and the exigencies of war

Don’t mention the war! Not this time an episode from Fawlty Towers but the implied message during the Marshall-Serventy-Drysdale expedition around Australia in 1958. Despite having only one arm, ‘Jock’ Marshall had a distinguished record in the Second World War, leading a patrol behind Japanese lines in the New Guinea campaign. And he was clearly intent on winding up his great friend from Perth, Dom Serventy, on what he did for the war effort. Serventy, after a first degree from Western Australia, had acquired a Cambridge PhD with Frank Armitage Potts (1882-1937)—the ‘P’ in the famous book on invertebrates, BEPS, or as intoned in full, Borradaile, Eastham, Potts and Saunders. He then returned to Western Australia as a lecturer but in 1937 joined the fisheries division of CSIRO. And it was while working in fisheries that he became a hate figure to the Australian army. In Marshall’s words, the subject was raised one night during the airing of Ivan Carnaby’s ‘unsolicited views on army life and the evils thereof’. In Marshall’s words:

It was at this camp that we got some understanding of an affair that had been bothering some of us for several years past. Looking at Dom's face—a face benign in repose as he contemplatively swigged at a pannikin of rum and water in his swag near the fire—it was difficult to believe that here was one of the men most detested in the Pacific Theatre during the war against the Japanese. There was little about him now that would suggest that Dom was one of a group of persons whom many people wanted to indict as war criminals. Generally, if one is unfortunate enough to find oneself in the company of such a person, one tends to avoid like a plague the subject of former contention. But we had heard so many conflicting stories about the part that Dom had played in this unsavoury business that we felt that this would be a good opportunity to let him talk about it and, if he chose, to offer an explanation to us, an essentially sympathetic audience.
So in our tactful way we said suddenly, ‘Tell us about your part in that rather disagreeable goldfish business during the war, Dom.’
There was silence, except for the crackling of the fire. Ivan, a close friend of Dom's, and once a soldier, stirred uneasily.
‘It was not goldfish,' said Dom quietly. ‘The fish is Nematalosa erebiya so-called bony bream. It is, in fact, a true herring—one of the soft-rayed clupeoid fishes. It is a Perth fish, and therefore a good fish.'
There was another silence.
‘It is true,' Dom started off again, ‘that it does not command any sale when fresh. But is nevertheless a very fine fish, and it can be caught easily in great numbers by means of mesh nets of the beach seine type in the Swan River, the Leschenault Estuary and elsewhere. Leschenault was one of Peron's men in Baudin's expedition of 1801.' 

‘It would be rather pleasant if you didn't change the subject,' somebody said. 

‘Well,' resumed Dom, with some dignity, ‘in World War II, Mr A. J. Fraser, Director of Fisheries, whom you have met, suggested to Mr Vincent Gardiner, whom you do not know, that as he was already engaged in the production of turtle soup, it might be extremely helpful to the war effort if he, Mr Gardiner, experimented with the canning of certain common Western Aus­tralian estuarine fishes, particularly Perth herring, for which there was no demand when fresh. It turned out to be a very good product,' concluded Dom, a little defiantly. 

‘But how did you get mixed up in these criminal activities?’ somebody broke in. 

‘I was transferred home to Western Australia during the war to work on, among other things, the biology of the Perth herring, ‘It turned out to be a very fine fish. Not perhaps of the quality of good Scotch salmon, but nevertheless, a very good fish and, in tomato sauce, very similar to European herring.
‘It is true, unfortunately, that the flesh is comparatively soft. Therefore it does not stand excessive handling during transport. When tins of Perth herring eventually reached the forward troops the fish was still tasty, but appearances were against it. 

‘Irrationally, the privates objected.’
‘Various personages associated with this delectable product, notably A. J. Fraser, Vincent Gardiner and myself went in some danger of our lives.’ 

‘It was even suggested that we be arraigned before the war criminal courts on charges of having conspired with the Japanese to lower morale.’

‘This charge is not true.’
There was silence except for the crackling of the campfire.
‘It was an attractive product, I thought,’ said Dom.
‘I enjoyed them.’
‘It was an honest attempt urgently to step up production of a food in short supply.’
‘How were we to know they wouldn't travel?’
‘We did our best.’
‘I would accept a tin of this fine Perth fish any time.’

I think we can take it that Jock Marshall, deep in the tropical jungle of northern New Guinea, was perhaps not terribly impressed by the odour, flavour or consistency of a disintegrating detritus-feeding fish in tomato sauce.

Perhaps then not surprising that Serventy moved to the wildlife division where he could pursue his lifelong interest in birds.

Perth Herring

The fish in question is now known as Nematalosa vlaminghi and it goes under the common names of Perth Herring, Bony Bream (but not to be confused with N. erebiya also known by that name) and Western Australian Gizzard Shad. It spends a period feeding at sea and then migrates to spawn in estuaries. Vincent Gardiner had a factory, Ocean Canning Company, at Belmont, Perth. Born in Dorking, Surrey in 1893 and educated at Reigate Grammar School, he began his career at sea as a radio operator. He then became superintendent of the Marconi School of Wireless in Sydney. A move as sales manager of Amalgamated Wireless also in Sydney was followed by his starting a gasket and felt company in Brisbane and Sydney. In 1937 he moved to Perth and began a meat canning company. It was there that he met A.J. Fraser and, as explained by Serventy, set up a canning factory for Perth Herring. The Australian army contracted to buy his entire output.

Although Gardiner moved into other lines, he was continuing to can Perth Herring for the civilian market into the 1950s. The tins were sold in Western Australia under the ‘Seahaven’ brand but production was insufficient to market them elsewhere. In a brochure extolling the virtues of Belmont, a former factory worker recalled his time working for Gardiner from 1940:

My original job involved cleaning fish, these being Perth Herring. The local fishermen received one penny per pound for them and cleaning was usually done by women who were also paid one penny per pound.

I wonder how Perth Herring in tomato sauce compared with my weekly lunch of sardines on toast or that dish still popular with Brits of a certain age, tinned pilchards?

Marshall AJ, Drysdale R. 1962. Journey among Men. London: Hodder & Stoughton. Paperback: Melbourne: Sun Books 1996 (reprinted 1967 (twice), 1968).

JOURNEY AMONG MEN by Jock Marshall and Russell Drysdale. A zoological/nuclear fallout expedition around Australia in 1958

Although I have written about him in previous articles on this site, have read some of his papers, have seen some of the press cutting about him and been in his first lieutenant’s department for a while, I had not read any of Alan John ‘Jock’ Marshall’s (1911-1967) books. The first to arrive was Journey Among Men, first published in 1962. I was pleased it was the first since I was intrigued by what the collecting expedition, which covered much of western and southern Australia it describes, was all about. I was also interested in his description of places we had been to in the Kimberley region of Western Australia 60 years later.

The real reason for the expedition was only alluded to in the book and I will return to the background later. Much greater emphasis is placed on the people, places, animals and plants encountered while travelling the vast distances and camping most nights. The book itself is an extended compilation of articles Marshall wrote for a Sunday newspaper, The Observer. Writing was completed when Marshall had moved back to Australia—to the then new Monash University in Melbourne, from London. The expedition though started in September 1958 when he was still Reader in charge of the Department of Zoology at St Bartholomew’s Hospital medical school.

The route of the expedition. The first party started at Perth and the second in Sydney.
They met at Fitzroy Crossing in the Kimberley region of Western Australia

The members of the expedition were, apart from Marshall himself:

Dominic Louis Serventy (1904-1988), an outstanding ornithologist, at that time in the wildlife survey section of the Commonwealth Scientific and Industrial Research Organisation in Perth. He collaborated with Marshall in research on the breeding cycles of birds and he, with Marshall, began planning the expedition in 1957.

Kenneth Gordon Buller (1915-1995), collector, ornithologist and taxidermist. Buller was senior preparator at the Western Australian Museum. He returned to Perth after the survey of Montebello and Barrow islands.

They, with Marshall, set out from Perth on 11 September in Serventy’s Land Rover and trailer. 310 miles north at Yalgoo they were joined by:

Ivan Clarence Carnaby (1908-1974), farmer, naturalist and another noted ornithologist; he travelled in a battered Dodge ‘ute’ which Marshall, avoiding the Australian slang, spelt out in full as ‘utility vehicle’. He didn’t though go the full British and call it a pick-up. He returned home before the run south from near Port Hedland. Disliked ‘graduates, Yanks, bot-flies, snakes and Eastern Staters’.

That was the Western party. After working their way up, doing what they had to do on the way, they were to meet the Eastern party at Fitzroy Crossing, over 1,500 miles from Perth, in the Kimberley. The Easter party comprised:

Russell (Sir Russell from 1969) ‘Tass’ Drysdale (1912-1981). Artist and friend of Marshall. He added an account of the travels from Sydney, through New South Wales, Queensland and Northern Territories to Fitzroy Crossing as well as providing drawings of the people met on the journey among men; the drawings illustrated the articles for The Observer, as well as the book. With him was his son:

Tim Drysdale, employed by Marshall as a helper to the expedition.

Jane Marshall described the circumstances:

It was on this journey that Jock and Tass discovered the depth of their friendship. It was in part due to the troubles of Tass's son Tim, whom Jock was employing for the rest of the trip as mechanic and general helper. He had deep compassion for the sense of helplessness and sadness Tass felt in not being able to reach his son emotionally or guide him out of his difficulties.

The Drysdale story did not end well: Tim Drysdale killed himself in 1962, the year the book was published; his mother followed a year later.

A fly-in, fly-out member of the expedition was Donald Sankey Farner (1915-1988). He was then Washington State University at Pullman but in 1958 he was spending a year in Perth on a Guggenheim Fellowship working with Serventy on the control of the reproductive cycle in the Zebra Finch. He was one of the key players—along with his friend Marshall—in lifting ornithology from its traditional descriptive focus to a broader base including how birds work. Thus his ‘avian biology’ has a very different connotation compared to ‘ornithology’. Don Farner—the only member of Marshall’s expedition I knew or met—arrived by air near Fitzroy Crossing and left, from my reckoning of he description of the book from Marble Bar airport near the start of the road south that leads south to Kalgoorlie. Farner came into a great deal of ribbing by the Australians because he always used pills to sterilise his drinking water—and doubled their number when dead pigeons were found in a water tank from which they had filled their bottles.

No member of the expedition travelled the whole distance. Russell and Tim Drysdale travelled the longest distance, starting and finishing at Sydney.

Why the expedition?

The 1950s was everything nuclear: from nuclear power and nuclear weapons to nuclear medicine and the use of radioactive isotopes in biological research. The intended research of the expedition seems to have depended on three strands: (i) Marshall’s own interest in the factors controlling seasonal reproduction; (ii) Marshall’s befriending of Joseph Rotblat at Barts Medical School, (iii) reports of the appearance in Kenya and Britain of some migratory birds in nuptial rather than eclipse plumage; the birds that had arrived in Britain were found to contain radioactive isotopes from nuclear weapons tests.

The whole story about plumage and radioactivity is told in the 12th Annual Report of the Wildfowl Trust for 1959-60 in an article by JM and RG Harrison:

The first suggestion that birds were being affected by radioactive fallout was made by Mr. John Williams, Ornithologist to the Coryndon Museum, Nairobi, who wrote to The Times in December 1955 stating that certain wading birds had appeared that autumn in Kenya in what appeared to be fresh summer plumage, the species in question being Greenshank and Sanderling. He commented that “It makes one wonder if these birds have been in a radioactive area in northern Russia, which has somehow affected their moulting sequences.”

On 9th November of that same autumn we had collected a female Redshank of the Icelandic race on the Medway Estuary in Kent (Harrison and Harrison 1956a), which was already in advanced freshly-moulted summer plumage, the breast and flanks being heavily spotted and streaked and the back, the head and neck showing the black streaks and barring of summer, the whole plumage being strikingly different from another female in normal winter plumage, which was shot on the same day. It is well known that some gonadal recrudescence occurs in autumn and this is responsible for autumn song and courtship, in such species as the Chaffinch, Song-Thrush, Dunlin, Redshank and Mallard, but we could not trace any record of a wading bird actually assuming summer plumage.

Following the exhibition of the Icelandic Redshank at a meeting of the British Ornithologists’ Club, consequent upon Mr. Williams’ remarks in The Times, arrangements were made with Dr. John Loutit of the Radio­biological Research Unit of the Atomic Research Establishment at Harwell for the examination of the bones of any further birds suspected of radioactive contamination. On 24th December, 1955 a further Redshank (Harrison and Harrison, 1956b) was obtained at Rye Harbour which showed incipient summer plumage and on dissection the ovary and oviduct were more fully developed than is normal in individuals collected at that time of year. Part of the skeleton was therefore sent to Harwell where it was dissolved in nitric acid and the presence of radioactive contamination was confirmed by Dr. G. E. Harrison and Mr. W. Raymond using a Veall Geiger Counter, and a graph prepared of the decay of the skeletal activity over the next two weeks. Dr. Loutit’s report stated that “ at least it proves that the bird had been exposed to some radiation,” but he went on to add that of course in a series of one there is no control. The ovary and oviduct were submitted to Dr. A. J. Marshall who reported that “the slides show quite clearly that the bird has become sexually advanced. You will see that the oocyte diameter (in the largest cases) is somewhat in excess of what would be expected for an ordinary wintering bird. This probably connotes oestrogen liberation. The oviducal proliferation is of course a consequence of oestrogen liberation.”

Dr. Loutit thought that the effect, although it appeared like a stimulatory action of radiation, was more likely to have resulted from an initial depression and a subsequent rebound phenomenon; the radiation first depressing cellular activity and thus delaying the assumption of summer plumage, and then as the effect wears off, the bird going into breeding plumage as a late phenomenon and out of its proper season.

So that is how Marshall became involved. Clearly though he was talking to his opposite number in the Physics department, Joseph Rotblat (1908-2005). According to Rotblat’s biographical memorialists for the Royal Society, for a time after his appointment to Barts the only person who would talk to him was Marshall. I cannot deduce whether this was because of Rotblat’s controversial past in the development and then repudiation of nuclear weapons or because he was not medically qualified; either or both could be the case. At this time Rotblat (later Sir Joseph and winner of a Nobel peace prize) was working on the biological effects of radiation and it is easy to envisage he and Marshall cooking up a scheme to study the effects of radiation on reproduction in birds.

The studies were funded by the Nuffield Foundation and, as explained in a news snippet in New Scientist (23 October 1958) the approach was two-pronged:

Suspecting that radiation may have upset the sexual cycle, Dr. Marshall is to collect several hundred fish, amphibians, reptiles, birds and mammals in different parts of Australia exposed to different amounts of radioactive fallout. A colleague, Dr. Brian Lofts, will carry out laboratory experiments on African weaver-finches, chosen for their periodic plumage changes.

The sites with the most exposure to radioactivity were of course those used for the British atomic weapons tests in the 1950s: Trimouille and Alpha islands in the Montebello archipelago off north-western Australia (1952 and 1956); Maralinga (1956, 1957) in South Australia. The visit to Montebello hardly gets a mention in the book, other than: ‘And on one of the Monte Bellos, a whole hillside, scorched by the incredible blow-lamp of an atomic bomb, testified to the most recent visitation by man’. There is a little more information in Jane Marshall’s write-up of her husband’s biographical notes:

Jock had a geiger counter and on Trimouille Island went ahead 'a little wary of the bay in which the guineapig ship was blown up in the first explosion.' They found the whole cliff-face scorched by that 'incredible blow-lamp of the atom bomb', then came to the slightly radio-active huts in the probable fall-out area as mapped for them by the people at Aldermaston in England, who were extremely interested in the investigation. There was not much more radiation than given off by Jock's watch until they came to what was probably wreckage from the ship. This was very active. 'We collected 42 terrestrial vertebrates on the islands, retaining the skins for the W.A. Museum & preserving the bodies for analysis at Bart’s.'

and:

On the way [to the Kimberley] they were collecting vertebrates in an arc around the Monte Bello area for shipment to London.

By the time the expedition came to Maralinga, there were only three members left: Marshall and the two Drysdales. Again, the work there was passed over in two sentences: ‘The work on which we were engaged at Maralinga has no place in this story. We spent some time at the base where we slept in sheets, went to motion pictures whenever we wanted to, ate ridiculously good food and used base facilities to overhaul the truck’.

Jane Marshall expanded thus:

Maralinga was Jock's most important goal. They arrived on October 28th and found 'a swimming pool, a change of picture show every night, tennis courts & superb cooking in the Commander's mess, where I am.' He found he had met the Commander and Chief Administration Officer during the war. This was another world from the one where they carried their water and selected their camps according to the firewood supply. Issued with protective clothing and placed in the charge of a security officer Jock went about collecting '313 terrestrial vertebrates in specifically "dirty" areas and in “clean" areas nearby. As before these included mammals reptiles and ground birds ... Of the Maralinga material some reptiles showed a count significantly higher than that of the background.' 

Outcomes

I have searched without success for reports on the results of monitoring animals for radioactivity. Was this because nothing of interest was found or because, which must have been the case in Maralinga, security clearance must have been obtained and the results treated as confidential? Grantees write reports on how they had spent their funds (I have one John Phillips wrote to the Nuffield Foundation on his funding for comparative endocrinology in Hong Kong) and I wonder if there is anything in the Nuffield Foundation’s archives. Jane Marshall mentioned that Aldermaston (Atomic Weapons Research Establishment) was interested in the results. Was a report sent there?

By contrast, two papers were published by Brian Lofts (1929-2015) and Joseph Rotblat on the direct, experimental approach to studying the effects of radiation on birds. Effects on the testis and on the regeneration of feathers after exposing Red-billed Queleas (Quelea quelea) to x-rays were found. While the results were interpreted as suggesting that irradiation had upset the pituitary cycle which controls the onset and loss of breeding plumage—as originally proposed for the appearance of birds in breeding plumage in Kenya and England after migration—the results were not followed up and several interpretations are possible for the appearance of a black band in the regenerated feathers of irradiated female queleas.

I suspect that little was achieved by Marshall’s expedition in relation to its original purpose. However, it is clear that the opportunity was taken to survey the wildlife in Western Australia and I have found that a CSIRO report was written by Serventy and Marshall: A natural history reconnaissance of Barrow and Montebello Islands 1958. Farner also clearly, as described in the book, took the opportunity to extend his work with Serventy on the control of the breeding cycle in the Zebra Finch.

Jock Marshall also spent time in Australia scouting out potential jobs for a return there from London. He, in the ultra-conservative world of Australian universities, and a self-confessed former larrikin was considered rumbustious and, as I explained in an earlier article, had acquired an influential sworn enemy as a result of the Golgi War. Eventually though he was offered a chair in the new Monash University and it was there that the book was written. How the people of Adelaide and Melbourne—the ‘wowsers’—greeted Marshall’s definition of the term (‘a gentleman who uses a contraceptive as a book-mark for his Bible’) greeted his return—or the book— is not recorded.

Journey among Men

The Marshall-Drysdale book is a fascinating account of life in the outback in the 1950s through the eyes of a thinking Australian zoologist who had spent many years in Oxford and London. To have followed in the expedition’s footsteps 60 years later at Winjana Gorge, Tunnel Creek, Hall’s Creek, Fitzroy Crossing, Geikie Gorge, Derby and Broome was equally interesting. For some places like Geikie Gorge and Tunnel Creek Marshall’s description still fits; for others like Broome, the place and people have changed beyond all recognition. Well almost, because visitors, even poms, will come across some old boy with a tale to tell. But the days must have gone when a notice could be seen on the pub wall in Port Hedland:

Whispering Smith has taken out an order restraining Billy the Lurk from drinking intoxicating liquor for a period of three months.

------------------------------------------------

The following are a few of Drysdale's illustrations for the book:

This is the poignant back cover of the 1968
paperback edition of Journey among Men

A view in the Kimberley, 2018

Marshall AJ, Drysdale R. 1962. Journey among Men. London: Hodder & Stoughton. Paperback: Melbourne: Sun Books 1996 (reprinted 1967 (twice), 1968.

Marshall Jane. 1998. Jock Marshall: One Armed Warrior, Australian Science Archives Project, Melbourne.

Harrison JM, Harrison JG. 1961. Radioactive contamination in birds. Tweflth Annual Report of the Wildfowl Trust 1959-1960, 151-152.

Hinde RA, Finney JL. 2007. Joseph (Józef) Rotblat. 4 November 1908 — 31 August 2005. Biographical Memoirs of Fellows of the Royal Society 53, 311-326.

Lofts B, Rotblat J. 1960. Effects of wholebody irradiation on the breeding plumage of the weaver finch, Quelea quelea. Nature 187, 615-616.

Lofts B, Rotblat J. 1962. The effects of whole-body irradiation on the reproductive rhythm of the avian testis. International Journal of Radiation Biology and Related Studies in Physics, Chemistry and Medicine 4, 217-230.

Chinese Mountain Cat: New research indicates it is a subspecies of the Wildcat

After our encounters with Chinese Mountain Cats in Sichuan in 2017, I wrote several articles on this enigmatic and attractive small felid (here, here, here). Over the years, the origins and status of this cat have been discussed. In essence, the argument has been whether it is a full species, Felis bieti, or a subspecies of the Wildcat, here called Felis silvestris. At the time I wrote those articles the view that appeared to prevail was that since it had been reported that the ranges of the Chinese Mountain Cat and the Wildcat overlap, i.e. they are sympatric, they must, therefore, be two different species.

These photographs of a Chinese Mountain Cat were taken by Tim Melling
in 2019 in the same location we (with Tim) saw them in 2017.
This one was crouched next to the road and he took this photograph
from the car using torchlight in the pitch dark. The light blue eyes
and the ear tufts can be seen. Note the thick, unpointed bushy tail.
I wonder if this is the same cat as the one I videod at long range
as it patrolled the grassland in 2017?
These are from Tim Melling's Flickr pages here

The Chinese Mountain Cat was first described by the Frenchman of British descent and English surname, Alphonse Milne-Edwards, in 1892. At the time Milne-Edwards was the new Director of the Muséum National d'Histoire Naturelle in Paris. He named the cat, collected in Sichuan, as a new species, Felis bieti, after the French missionary and naturalist, Félix Biet (1838-1901).

Before describing the latest research I must point out that the taxonomy of the various forms of Wildcat in Eurasia and Africa has been the subject of constant change. I am following the authors of the current paper in calling the Wildcat of Europe and parts of Asia, Felis silvestris with five distinct interfertile subspecies or geographical forms, the one in northern China being Felis silvestris ornata. An alternative scheme from 2017 lumped the Wildcats from Africa and Asia into one species, Felis lybica; in that scheme the Wildcat of northern China is Felis lybica ornata. However, that wider problem of Wildcat classification is not germane to the present research on the status of the Chinese Mountain Cat and its relation to the northern Chinese form of the Wildcat.

This week a new paper appeared in Science Advances which specifically addresses the status of the Chinese Mountain Cat. A group of authors from China, Malaysia, Russia and the USA have done a phylogenetic analysis of zoo, museum and villages-kept specimens using nuclear and mitochondrial DNA sequences of 27 Chinese Mountain Cats, 4 Wildcats of the form found in China (Felis silvestris ornata) and 239 domestic cats.

From the phylogenetic analysis, the authors conclude that the Chinese Mountain Cat, which occurs only on the Qinghai-Tibet Plateau, is not a separate species but a subspecies of the Wildcat with a past and complex history of hybridization between the two. Surprise, surprise: Mountain tom cats spreading their genes into the Wildcat population and the offspring back-crossing into the Mountain population appears the most likely explanation for the hybridization events at a time when the ranges of the two forms overlapped. Evidence of extensive past genetic exchange between the two lineages and therefore interbreeding was found

The authors also address the question of whether this conclusion from nuclear and mitochondrial DNA is also compatible with ‘the biological species concept, which considers interbreeding as the prerequisite for a species. The key argument from the proponents for the species status of the Chinese mountain cat lies on its distinctive morphological characters, a presumed sympatric distribution with the Asiatic wildcat, and an absence of gene flow between free-ranging Chinese mountain cats and Asiatic wildcats. However, recent surveys in Northwest China showed that the range attributed to the Asiatic wildcat may have been overestimated and that its presumed presence on the Qinghai-Tibet plateau in north-eastern Qinghai may not be true. That assertion, if proven, would dispute the supposed sympatry of the two lineages’

Differences in appearances were noted in genetically-determined hybrids. For example, the tail was less bushy in a cat with the nuclear DNA of a Mountain Cat and the mitochondrial DNA signature (passed down the maternal line) of a Wildcat. The presence of hybrid cats (i.e. crosses with Wildcat or with domestic cat—see below) could explain the seemingly anomalous appearance of some cats seen and photographed on the Qinghai-Tibet Plateau in recent years.

The authors continued in their conclusion on the Mountain Cat:

Answers to the remaining questions require more surveys and studies to fine map the Asiatic wildcat and Chinese mountain cat distribution in Northwest China; to delineate the subspecies boundaries or hybrid zones; to elucidate the ancestry, adaptation, and evolution of these taxa; and to resolve the historical and current patterns of gene flow among the wildcat and domestic cat lineages in the region.

Will the status and origins of the Chinese Mountain Cat and the other Wildcats of Eurasia and Africa now be regarded as settled? I wouldn’t bet on it although at the moment the ‘lumpers’ certainly hold sway.

The point the authors make on evidence of recent cross-breeding with domestic cats has major implications for the conservation of the Mountain Cat, as the authors explain:

Contemporary genetic introgression from F. s. bieti into sympatric domestic cats is evident across, but not beyond, the range of F. s. bieti. The timing of admixture coincided with large-scale socioeconomic changes in the Tibetan area during the mid-20th century. That process likely led to an expansion of domestic cats into the region and suggests that domestic cats arrived rather late to the Plateau and thus had not encountered F. s. bieti until recently. The increasingly abundant local domestic cat population may pose a threat to the Chinese mountain cat and jeopardize its genetic integrity and evolutionary adaptation to high altitude, an issue with profound conservation implications and worth further study.

Those of us who live in Scotland will recognise the same conservation and taxonomic problems with the Scottish form of the Wildcat. Firstly, survival in the wild is severely threatened by cross-breeding with domestic cats. Secondly, the status of the form has varied from being considered a species (Felis grampia) a separate subspecies of the Wildcat (F. silvestris grampia) or lumped into the European Wildcat (Felis silvestris silvestris). I read that the latter is the currently favoured view.

On that note of deep concern for the future integrity of the Chinese Mountain Cat, the present data supporting ‘lumping’ of the Felis cats mean China loses an endemic species from its faunal list but gains yet another conservation problem.

He Yu, Yue-Ting Xing, Hao Meng, Bing He, Wen-Jing Li, Xin-Zhang Qi, Jian-You Zhao, Yan Zhuang, Xiao Xu, Nobuyuki Yamaguchi, Carlos A Driscoll, Stephen J O’Brien, Shu-Jin Luo. 2021. 

Genomic evidence for the Chinese mountain cat as a wildcat conspecific (Felis silvestris bieti) and 

its introgression to domestic cats. Science Advances 7 (26), eabg0221. DOI:10.1126sciadv.abg0221 

The Reptile House at London Zoo: the beginning of the end

News that London Zoo was to start the process of planning a new reptile house appears to have evoked little response other than in the zoo enthusiast community which, in general, has expressed regret at the loss of the old one. The plan, as reported, is for the new one to hold only 29 species—all for captive breeding of species of conservation concern, plus a new house for Galapagos tortoises, while the old house is to be retained for purposes yet to be decided.

Views of the current Reptile House have varied over the decades from its opening in 1927. It was groundbreaking in terms of design, control of environmental temperatures and provision of ultraviolet radiation but a common view in the 1950s and 60s was that it was a deathtrap for its reptilian inhabitants (it had soon been established that it was too hot for many amphibians). Design of the house was attributed by the besotted Peter Chalmers Mitchell to Joan Procter with the architect Guy Dawber being demoted in importance to having added the fancy bits. By contrast, Solly Zuckerman thought Joan Procter overbearing, over-rated and over-promoted.

Entrance to the Reptile House, 2011
Photograph by William Hook via Wikimedia

Original plan of the Reptile House
The Times 15 June 1927

It is true that the mortality rate of reptiles at London Zoo was very high in the early decades of the reptile house’s existence. in 1946-48 the annual death rate was 45.4%; in 1956 it was 68%. In other words two-thirds of the inhabitants were dying within the year. I do not know the extent to which the environments afforded by the house were responsible. However, it is worth pointing out that many reptiles and amphibians arrived from abroad both for zoos and animal dealers in very poor condition. Animals were often unfed and unwatered for long periods and kept in crowded, unsuitable conditions before being shipped. Reptiles take a long time to die and can reach a stage of irreversible metabolic damage. No matter how well they were treated on arrival the outcome was inevitable. The great advances in reptile husbandry (and in the veterinary treatment of wild animals) of the 1970s and 80s was still to come. From being unable to breed nearly all species in the 1950s, private herpetologists led the way in devising the means of doing so. Zoos generally followed that lead but it was clear that the Reptile House was not ideal for use as a breeding setup even with the best efforts of the keepers at the time. Furthermore, the building was getting tired with much of the old equipment unusable; for long periods of its existence there was not enough money available for even minor improvements. Even 20-30 years ago it was evident to many of us that the Reptile House needed to be replaced in order to provide accommodation commensurate with the great advances made in keeping reptiles during the 1970s and 80s and with providing staff with better facilities for incubation of eggs and the raising of young animals to adulthood together with showing visitors these processes in action.

I am therefore delighted to hear the plans for a new reptile house. I do though share the concern of comments I have read that plans are being made for only 29 species. That announcement cuts to the heart of the matter about the role of zoos in the 21st century. Should the collection comprise only those species in actual or potential need of captive-breeding programmes? Or should they be there to educate the public about the diversity of animal species? How much public ‘entertainment’ in the way of common but popular species or ‘immersive’ exhibits is it necessary to include in order to attract the paying public in sufficient numbers and thereby support financially the conservation and educational efforts within the zoo and in the wider world?

These strategic questions and the arguments for and against each scenario are not new and will continue to engage informed—and much uninformed—opinion. On the ground it is difficult for the majority of zoo visitors to appreciate how many of what were major collections, including London Zoo, have destocked in terms of number of species and of individual animals kept. Keeping the discussion to reptiles and amphibians, in the years 1949-51 London Zoo had 221 species; in 1957 there were 168 while in 2020 the number was 59.

What concerns many people I know is the lack of a comprehensive collection of reptiles and amphibians in Britain. With so few native species, these animals are the least known and, despite decades of educational effort, the most reviled. They need to be seen in the flesh in all their diversity. Television just does not cut it. There is a real opportunity for imaginative displays, some with ‘reversed daylight’ to show the diversity, adaptations and breeding of reptiles and amphibians and why they are an important part of the natural world.

The days though of going to the Reptile House first to see what was happening and what was new—a common trait amongst many of us whose first interest was reptiles and amphibians—seem numbered.

Masai Mara Safari - 30 years ago

Itchy feet with the world out of reach? These photographs from the Masai Mara in September 1991 will not help.

Black Rhinoceros

Topi (Damaliscus lunatus) with Thomson's Gazelles (Eudorcas thomsonii) on the right.
Landscape typical of the Masai Mara

Lioness

Cheetah

...only moved slightly when we passed by later

Marsupial frogs: Important questions remain on life in the pouch

Following up my article on marsupial frogs, I have acquired a copy of William Duellman’s book, Marsupial Frogs. Gastrotheca and Allied Genera published in 2015¹. Book hardly does the work justice because it a complete account, based on five decades of research by the author, particularly on their taxonomy and evolution, of this remarkable group of South American amphibians. As well as general chapters on aspects of their biology, each species is described in detail. Duellman began his book as follows:

What are marsupial frogs, and why are they so particularly worthy of study. These are the only frogs in which males fertilize the eggs out of the water and then place them in a pouch on the back of the female. The developing embryos of marsupial frogs and their allies—i.e. the amphibian family Hemiphractidae—have large external bell-shaped or sheet-like gills that are unlike those of any other lineage of frogs. These behavioral and developmental features are unique to marsupial frogs and their allies.

The first point I wanted to check was what he had to say about the identification of frogs exported from South America in the 1950s, presumably through the animal trade. These animals were the basis of early work on reproductive behaviour and the use of the dorsal sac to hold fertilized eggs. As I stated in my previous article, the frogs are now thought not to have been Gastrotheca marsupiata or marsupiatum as they were labelled at the time, but G. riobambae from Ecuador. Duellman in his book repeats the sorting out of this misidentification but also adds that another species, G. pseustes, very similar in appearance to G. riobambae, also occurs in the Andes surrounding Quito; that species may have been also have been involved in the exports and studies.

Getting the species right is important in the these frogs (69 species recognised in the genus Gastrotheca at the time Duellman’s book was written) because the stage of development at which the young emerge from the pouch on the mother’s back differs. In a few species, incidentally, the pouch is on the side and even extends via a slit into the abdominal cavity. Some hemiphractid species, all in genera other than Gastrotheca, have no fully enclosed pouch: some have a dorsal patch to which eggs adhere; others have a basin-like structure while in one genus, the eggs are enclosed but the two edges of the skin flaps forming the cover do not fuse.

From Duellman's book

In species such G. riobambae, G. marsupiata and G. pseustes the tadpoles when they hatch and shed their external gills leave the pouch (assisted by the toes of the female being inserted into the pouch) and continue their feeding, development and metamorphosis in ponds. The tadpoles, it should be noted, hatch at a more advanced stage than in species like the Common Frog. By contrast in some other species of Gastrotheca, the young hatch and emerge as fully-developed froglets; metamorphosis takes place in the egg capsule within the mother.

This is where things get physiologically more interesting. Marsupial frog tadpoles develop large external gills connected to the tadpoles by stalks. The gills have a large surface area and form, by analogy with mammals, the fetal side of the placenta. The brood pouch is formed from skin but internally loses loses much of the structure typical of skin when eggs are in the pouch. The epidermis becomes thin and produces well vascularized extensions that partially envelop the egg. In other words, the skin forms the analogue of the maternal side of the mammalian placenta. Between the two sides is the egg capsule across which any exchange or transfer of materials between mother and egg/tadpole must occur. It is obvious that oxygen must pass from mother to egg/tadpole with carbon dioxide moving in the reverse direction. The form of the nitrogenous waste produced by the tadpoles shows an interesting adaptation. Free-living tadpoles usually resemble fish in that they produce ammonia—they are ammonotelic—which being toxic is swiftly excreted into the surrounding water; at metamorphosis terrestrial amphibians switch to produce urea. However, marsupial frog tadpoles produce urea—they are ureotelic—and not ammonia. Not all the urea though leaves the egg capsule. It has been suggested that the urea could serve some osmotic function (as in the Crab-eating Frog) and preventing the loss of water. This aspect required further study but the inclusion of urea in the culture medium made it possible to keep early embryos of G. riobambae alive after they were removed from the pouch; the usual saline solution was not sufficient.

Much of this work on the developmental biology of marsupial frogs has been done by Eugenia del Pino in Quito²; she has worked extensively on G. riobambae, and the aspects of her research described here only skim the surface of her studies done over the past 50 years on these fascinating frogs and their adaptations. Her research as a developmental biologist therefore complements that of Duellman, centred on evolution and taxonomy, over a similar period of time.

The big question, of course, with marsupial frogs is whether or not the developing tadpoles draw on maternal nutrients to support their growth and development in addition to the nutrients provided at the time of laying in the yolk—the eggs of marsupial frogs are very large and therefore contain a lot of yolk. In the tadpole-producing G. riobombae there is evidence that the developing tadpole relies solely on the yolk until it hatches and leaves the pouch. The weight of dry matter in the egg capsule was found not increase during development. By contrast, a more recent study³ on a froglet-producing species, G. excubitor, has suggested that maternal nutrients could be transferred to the developing young. However, having read the paper and having looked at the supplied raw data I remain unconvinced. The number of animals studied was very small at each stage of development; the embryos were only studied at early stages of development and the results of feeding stable carbon and nitrogen isotopes to prey insects, while indicating that carbon and nitrogen compounds (which could be simple products of metabolism like carbon dioxide or urea) pass from mother to embryo through the egg capsule, are not a demonstration of NET transfer of nutrients.

There do appear to be adaptations associated with producing froglets rather than tadpoles. Duellman provided a diagram showing that froglet-producing species have fewer, larger eggs (thereby providing evidence that the yolk is sufficient for development to froglet); eggs in the pouch are arranged in a single layer such that they can be completely enveloped in maternal blood vessels from both sides. By contrast, tadpole producers have more, smaller eggs, stored as a double layer in the pouch. All these findings are consonant with the increased requirements for oxygen in the later stages of growth and development by the larger tadpoles and metamorphs of the froglet producers.

In conclusion, the question remains—as it does for other frogs in which eggs are held in various body cavities until newly-metamorphosed froglets emerge—do maternal nutrients contribute to the metabolism and growth of the developing tadpole? The simplest way of answering that question would be to weigh the dry matter of the egg capsule and its contents right through the period of development in the pouch, as has been done in the tadpole-producing G. riobambae. We would then know if then know if the egg capsule with its rich supply of blood vessels on both sides acts in a manner more comparable with the mammalian placenta or if it just, as it says on the tin, just a gill. Molecular biologists might want to just have a look at whether or not transporters for glucose and amino acids occur in the egg capsule. 

The question of whether the external gill acts as a gill or an analogue of the mammalian placenta takes me full circle to my start of the first article and why Amo was fascinated by marsupial frogs and had a film made of their reproductive behaviour. There is still much of interest to do, with key questions still waiting to be answered, 65 years later.

1. Duellman WE. 2015. Marsupial Frogs. Gastrotheca & Allied Genera. Baltimore: Johns Hopkins University Press.

2. del Pino, EM. 2018. The extraordinary biology and development of marsupial frogs (Hemiphractidae) in comparison with fish, mammals, birds, amphibians and other animals. Mechanisms of Development 154, 2-11.

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