A New Matamata Species. Now there are two

The bizarre Matamata from South America was always thought of as one species, Chelus fimbriata. It did though seem odd that the one species is present in both the Amazon and in the separate river drainages in northern South America. In the 1990s some morphological differences were found in specimens from these distinct geographical regions. Now it has been established using both mitochondrial and nuclear DNA that the two populations separated about 12.7 million years ago, the time the Orinoco Basin in the north was formed. Matamatas living in the Orinoco and Rio Negro Basins and in the Essequibo drainage are morphologically and genetically distinct from those in the Amazon Basin and the Mahury drainage. The authors of the new paper have, therefore, split the old species into two: Chelus orinocensis from the former with C. fimbriata retained for the latter.

I have only seen one Matamata, other than those in zoos, and that was in the semi-wild state. During our trip to Guyana in 2006 we stayed for a couple of days at Rock View, a lodge in Annai on the Rupununi River, a tributary of the Essequibo. There in a large concrete tank lived a large Matamata which had been collected locally. The woman who looked after it climbed into the tank and lifted it out so that we could see and photograph it. This magnificent chelonian, which feeds  by sucking its prey into its mouth by a rapid expansion of the pharynx, was obviously of the newly described species, Chelus orinocensis.

Showing the location of Annai in Guyana. The Essequibo River reached the Atlantic to the north

  

Vargas-Ramírez M, Caballero S, Morales-Betancourt MA, Lasso CA, Amaya L, Martínez JG, Viana MS, Vogt RC, Farias IP, Hrbek T, Campbell PD, Fritz U. 2020. Genomic analyses reveal two species of the matamata (Testudines: Chelidae: Chelus spp.) and clarify their phylogeography, Molecular Phylogenetics and Evolution148, doi.org/10.1016/j.ympev.2020.106823.

Sánchez-Villagra MR, Pritchard PCH, Paolillo A, Linares OJ. 1995. Geographic Variation in the Matamata Turtle, Chelus fimbriatus, with Observations on its Shell Morphology and Morphometry. Chelonian Conservation and Biology 1, 294-300.

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Peter Dunn

I started to write this article a couple of days ago. That evening I found from Tim Melling a tribute on Flickr to Peter Dunn, the co-leader of that Naturetrek trip to Guyana, who had died earlier that day. Peter, a retired policeman from Scarborough, was well-known to birders in Yorkshire was well as to Naturetrek clients both as a leader and as compiler of those essential checklists. Our abiding memory is of Peter walking along a baking hot track wearing the Wellington Boots he had, after experience leading trips in Belize, wisely brought with him. With Flowers of Sulphur applied liberally to his thick socks he avoided the dreaded chiggers; the rest of the party did not.

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Why and how does an ‘annual’ chameleon die?

Laborde's Chameleon
Furcifer labordi
Christopher Raxworthy / Public domain

Twelve years ago came the news from Madagascar of an ‘annual’ chameleon—one that spent more time in the egg than as an adult.

In short, Laborde’s Chameleon, Furcifer labordi, was found to grow rapidly after hatching in November, to reach sexual maturity and breed by January-February and then to senesce and die. The adult lifespan was found to be 4-5 months. For the dry season of April to October there were no adults alive, just the eggs remained waiting to hatch at the start of the wet season in November.

The discovery excited a great deal of interest for all sorts of reasons. Not least was that among those studying the phenomenon and mechanisms of ageing, comparative life histories and longevity. Laborde’s Chameleon joined a few species of marsupials amongst tetrapods known to have a short lifespan and to die after a first breeding.

This is not the place to describe the large and controversial field of ageing. However, some of those involved may have been tempted to speculate that these short-lived chameleons might be exemplars of one theory of ageing which contends—erroneously in my view—that organisms have a built-in programme that, around a certain age, leads to death. However, what played on my mind, having once known a bit but never enough about chameleons, was what caused the chameleons to die after reproducing. Would they, for example, live longer if breeding did not take place? Was there something about the environment, a lack of food for example, that prevented their survival as adults?

A clue that Laborde’s Chameleon is not always strictly ‘annual’ came from a different location. Kirindy, where the warm, wet season is longer. There, females were found which had bred more than once and one survived into a second year after a particularly long rainy season. When these chameleons were kept in cages in the same region, some males were found to survive until the next season.

Still, I contend, the best way of looking at differences in lifespan between species is the Disposable Soma Hypothesis of Tom Kirkwood. In essence, because the availability of nutrients within the body is limited, animals balance the amount invested in reproduction and in repair. At one extreme, with Laborde’s Chameleon being an exemplar, the animal goes for rapid growth and reproduction at the expense of essential repairs to its cells, to its DNA, to fighting infection and infestation, to healing its wounds etc; as a result it dies when relatively young. At the other extreme, the slow-growing, slowly reproducing animal invests in keeping the adult in good condition for much longer; as a result it does not fall victim to tumours caused by errors in DNA copying or to infection and thus may live for a very long time; think elephant.

Thus, one might expect, with its defences down, Laborde’s Chameleon to fall victim to something in the environment that a longer-lived species which lives in the same habitat (like the Warty Chameleon, F. verrucosus, which aestivates during the dry season) would be expected to see off. I suggested some time ago to people in conversation that one of the factors that might be involved in the death of short-lived chameleons might be parasites. The reason I argued thus was that I had seen the incredible parasite loads of other species of chameleon after a short time in captivity: worms, protozoans and coccidial spores abounded. I was about to write this article when I came across a paper published in 2019 which examined that very idea—that a low resistance to parasites in Laborde’s Chameleon is what is the proximate cause of death of the adults.

The German group who reported the work from Kirindy joined forces with veterinary colleagues. They found that the parasite load in the alimentary canal increased dramatically during the last three months of life. Males had a greater parasite load internally and externally than females. Some animals were kept in cages—again in their habitat in Madagascar. Those individuals had a lower parasite burden and lived longer than their counterparts living in the wild. The authors concluded that the increased prevalence of gastrointestinal and blood parasites is entirely compatible with less investment in the immune system of these fast-growing, fast reproducing lizards—just as would be predicted from a trade-off between a rapid lifestyle and internal defence and repair.

Males might have been expected to be less affected than females producing eggs. However, it seems that males also put everything into reproduction. There is intense rivalry and bloody combat during the short breeding season as males guard their mates.

The indication of lower parasite loads in, and longer lifespan of, Laborde’s Chameleons kept in captivity in Madagascar suggests the need for further experiments. The animals were fed on invertebrates caught in the wild, some of which would presumably contain parasites. What would happen if, say, newly-hatched individuals were fed on parasite-free livefood? What would be their lifespan and what would they die of?

Finally, this article started off as one about a remarkable chameleon from a remarkable island fauna but it has to end as one about parasites and co-evolution with their hosts. In general, parasites evolve so as to be less lethal to their hosts. They have their own trade-off between going for growth and reproduction and killing the host by taking too much food and causing physical damage. So has co-evolution delivered a suite of parasites that like the chameleon itself go for broke and then in vast numbers lurk in an intermediate species for the onset of the next rainy season?

…and really finally. We did not see Laborde’s Chameleon when we were in southwest Madagascar in 2003. When I realised that was in October I now see why—the eggs were in the ground ready to start hatching in November.

Eckhardt F, Kappeler PM. Kraus C. 2017. Highly variable lifespan in an annual reptile, Labord’s chameleon (Furcifer labordi). Scientific Reports 7: 11397 doi:10.1038/s41598-017-11701-3 

Eckhardt F, Strube C, Mathes KA, Mutschmann F, Thiesler H, Kraus C, Kappeler PM. 2019.  Parasite burden in a short-lived chameleon, Furcifer labordi. International Journal for Parasitology: Parasites and Wildlife 10, 231-240. https://doi.org/10.1016/j.ijppaw.2019.09.010 

Karsten KB, Andriamandimbiarisoa LN, Fox SF, Raxworthy CJ. 2008. Proceedings of the National Academy of Sciences of the USA 105, 8980-8984. doi􏰊10.1073􏰊pnas.0802468105 

Stejneger’s Stonechat—in Hong Kong last week

From Hong Kong last week came this photograph of a male stonechat. Taxonomy of the stonechats of Eurasia is mighty complicated and this one is known at present as Stejneger’s Stonechat, Saxicola stejnegeri.

I say mighty complicated because to old Hong Kong birders this was called the Siberian Stonechat, S. maurus and sometimes as an eastern race of the Common Stonechat, S. torquatus. Since some of the evidence that recognises the form found in Hong Kong as a passage migrant and winter visitor from its breeding grounds in north-east China, is based on differences in mitochondrial and not nuclear DNA, I am not sure that the present taxonomy will hold sway for that long.

Stejneger was the Norwegian-born Leonhard Hess Stejneger (1851-1943) who made his name in the U.S.A. mainly as a herpetologist working at the Smithsonian. The pronunciation of Stejneger always offers a challenge to Brits. Here, apparently, is the way it should sound.

Beautiful bird.

How—and why—do tadpoles fill their lungs?

Those of us who have watched and kept tadpoles will have noticed that sometimes they come to the surface to take in air. A recent paper shows that very young and therefore very small tadpoles cannot break through the surface tension of the water in which they live. However, they still manage to take in air by a process the authors call ‘bubble-sucking’.

Even three days after hatching and only 3 mm long tadpoles have been found to fill their lungs. High-speed video showed what was happening. In five species of frog from North America and in the much-studied African Clawed Frog, Xenopus laevis the authors found: 

…mouth attachment to the water’s undersurface, the surface drawn into the mouth by suction, a bubble ‘pinched off’ within the mouth, then compressed and forced into the lungs. 

As tadpoles grow, they gain the size and strength to breach the surface of the water to take in air. However, larger tadpoles of one species studied (Grey Treefrog, Hyla versicolor) continued to use bubble-sucking exclusively while those of others used both methods until metamorphosis.

The authors recorded a similar of taking in air in salamander larvae which have external gills.

From Schwenk & Phillips 2020

It would be easy to assume that tadpoles take in air in order to extract the oxygen it contains. Tadpoles would normally be expected to respire through their gills and skin. With low concentrations of oxygen in the water, hot or fetid, for example, the selective advantage of being able to breathe air is obvious. However, the presence of air in the lungs is related to another function in these aquatic organisms—the control of buoyancy. I am surprised that the authors in their discursive account chose to concentrate on a presumed respiratory function when there has been a considerable amount published on air in the lungs in relation to the control of buoyancy. The authors themselves noted that in at least one of the species studied the lungs at 3 days after hatching are poorly vascularised and do not acquire a rich blood supply typical of a site of gaseous exchange until later in development. 

Tadpoles, by having the ability to fill their lungs with air using the newly discovered method of ‘bubble-sucking’ to overcome the surface tension of water, thus have the opportunity to use that air for the control of buoyancy and as a source of oxygen, depending on their stage of development and the degree of oxygenation of the water in which they live.

And I am still fascinated by tadpoles despite the strictures of my grandfather that I would never be able to make a living by studying them.

Schwenk K, Phillips JR. 2020. Circumventing surface tension: tadpoles suck bubbles to breathe air. Proceedings of the Royal Society B 287: 20192704. http://dx.doi.org/10.1098/rspb.2019.2704 

see also

Gee JH, Rondeau SL. 2012. Strategies used By tadpoles to optimize buoyancy in different habitats. Herpetologica 68, 3-13 doi.org/10.1655/HERPETOLOGICA-D-10-00023.1

The Coronavirus War: A quotation from an ace scientific adviser to government

Quoting from Solly Zuckerman, who pioneered operational research in the Second World War and who later became Chief Scientific Adviser to the British Government, might be appropriate in the present war against a novel virus in which scientific advice plays an even greater rôle:

One simply cannot order up so many assorted scientists to do a job, or command them to make a ‘break-through’. Operational prob­lems, I discovered, savoured more of the characteristics of biological enquiry than of those encountered by chemists or physicists. I had a fear that scientists who were accustomed to the handling of only strictly controlled situations, and who had little taste for others—for example, ‘pure’ mathematicians, or mathematical physicists, or theoretical biolo­gists—would have little to contribute to the solution of the kind of issues that were of overriding importance to the good military leader or politician… War generated an inflexibility of outlook, and the more remote from the scene of action, the more inflexible the desk warriors became. 

Pity, as an afterthought, I cannot find a quote about vulpine but scientifically illiterate journalists who labour an unimportant matter to advance their own or their organisation’s political agenda.

Solly Zuckerman
Tobruk, 1943

Zuckerman S. 1978. From Apes to Warlords. London: Hamish Hamilton, p 363

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

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

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

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

§Hong Kong Newt Paramesotriton hongkongensis

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

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

§Asian Common Toad Duttaphrynus melanostictus

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

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

§Paddy Frog Fejervarya limnocharis

§Chinese Bullfrog Hoplobatrachus rugulosus

§Günther’s Frog Sylvirana (Hylarana) guentheri

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

§Three-striped Grass Frog Hylarana macrodactyla

§Two-striped Grass Frog Hylarana taipehensis

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

§Rough-skinned Floating Frog Occidozyga lima

§Green Cascade Frog Odorrana chloronata

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

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

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

§Brown Tree Frog Polypedates megacephalus

§Spotted Narrow-mouthed Frog Kalophrynus interlineatus

§Asiatic Painted Frog Kaloula pulchra

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

§Ornate Pigmy Frog Microhyla fissipes

§Marbled Pigmy Frog Microhyla pulchra

G.A.C. Herklots

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

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

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

Paddy Frog (Fejervarya limnocharis)

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

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

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

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

Frogs of China. Alice Boring’s Life and Work. 2. Legacy: Liu Cheng Chao

Alice Boring made good use of her time on long leave in 1928-29. From correspondence with the leading American herpetologists of the day and by working at the American Museum of Natural History in New York she had, by the time she sailed back to China, compiled a checklist of amphibians from all parts of China. The checklist was published with Nathaniel Gist Gee (1876-1937)*. According to her biography she was instilled with what was then the American way of doing taxonomy: collecting a wide range of specimens over a wide area in order to determine the degree of variation within and between species. She established a network of people who sent her specimens as well as sending students and collectors on collecting trips to various parts of China. Because museums depend on access to specimens she sent and exchanged amphibians for study

Geoffrey Herklots at the University of Hong Kong, was, to go right back to the opening paragraph of Part 1, part of that network that existed throughout China and to the U.S.A. He sent collections of frogs to Peking for her to identify. In turn she published the findings in Hong Kong Naturalist.

Boring was a founder member of the Peking Natural History Society and it was in the the Society’s bulletin and a handbook that she published most of her work. However, it was not all taxonomy as some biographers have implied. One paper was on Bidder’s organ while another was on seasonal changes in the reproductive organs of frogs and toads, both continuing the sort of work she was doing in Maine before she left for China.

Liu Cheng Chou
from Contributions to the History
of Herpetology

Boring’s major legacy was a student Liu Cheng Chao (1900-1976). Not officially her student, Alice Boring provided advice and encouragement for Liu’s interest in amphibians at Yenching. After graduation, Liu lost his herpetological papers and books in 1931 when forced to leave Northeastern University at Mukden when the Japanese moved in. Boring took great trouble in  arranging for him to study for a Ph.D. in the U.S.A. funded by the Rockefeller Foundation. He went to Cornell to work with Albert Hazen Wright (1879-1970). Back in China, Liu was first at Suzhou University but the Japanese advance took him to Chengdu in Sichuan and the West China Union University. It was from there that he made 11 long field trips to the hills and mountains on the edge of the Tibetan Plateau. On one he was seriously ill with typhus fever. In September 1946 Liu returned to the U.S.A. and was based at what was then called the Chicago Natural History Museum, now the Field Museum of Natural History.

Liu was with some big names of classical herpetology in Chicago: Karl P. Schmidt, Clifford H. Pope and Robert F. Inger. Pope, of course, had travelled extensively in China and written a book on the reptiles. During his year there Liu wrote his major work Amphibians of Western China. Much more than a catalogue of amphibians it describes the field trips, the peoples he encountered and the geography. He discusses the adaptations of adults and tadpoles in relation to habitat as well as the history and cultural significance of the various species. It is not surprising that after this tour-de-force Liu was described as China’s most prominent herpetologist.

By the time Amphibians of Western China was published in 1950 (Liu’s Preface was dated 1 November 1948) he had returned to Yenching University as head of department. In 1951 he moved to Chengdu as President of Sichuan Medical College. He became a member of the Chinese Academy of Sciences. He and his wife Hu Shu Chin (Shu-qin) (1914-1992) later published Chinese Tailless Amphibians in 1961.

Liu acknowledge the part Boring had played in his career in Amphibians of Western China:

My former teacher at Yenching University, Dr. Alice M. Boring, has my grateful remembrance for her continued encouragement and help during the war years. 

In 1945 Liu named a spectacular amphibian, Vibrissaphora (now Leptobrachium) boringii in Alice Boring’s honour. This species is known as the Emei Moustache Toad because the males in the breeding season have sharp tubercles around the upper lip. These spines are used in defence of their nests. A frog full of vim and vigour named for a ‘dame full of vim and vigor’. And, surely, it should have the common name, Boring’s Toad?

A plate from Liu's book showing the species named for Alice Boring
I have added a red arrow to show the sharp tubercles

Another plate from Amphibians of Western China

A modern photograph of Boring's Toad
from Hudson & Fu 2013

*Yenching University had, incidentally, originally lined Gee up for Boring’s job when he was free to take it. That is why she was only offered a two-year appointment.

Anon. 2014. Boring, Alice M. In Contributions to the History of Herpetology (Volume 1, revised and expanded), Edited by Kraig Adler, pp 107-108. Society for the Study of Reptiles and Amphibians.

Anon. 2007. Hu, Shu-qin (1914-1992). In Contributions to the History of Herpetology (Volume 2,), Edited by Kraig Adler, pp 207-208. Society for the Study of Reptiles and Amphibians.

Anon. 2014. Liu, Cheng-chao (1900-1976). In Contributions to the History of Herpetology (Volume 1, revised and expanded), Edited by Kraig Adler, pp 123-124. Society for the Study of Reptiles and Amphibians.

Fu L. 2017. Nathaniel Gist Gee’s contribution to biology in modern China. Protein & Cell 8, 237-239 DOI 10.1007/s13238-016-0318-x 

Hudson, CM, Fu, J. 2013. Male-biased sexual size dimorphism, resource defense polygyny, and multiple paternity in the Emei Moustache Toad (Leptobrachium boringii). PLoS ONE 8(6): e67502. doi:10.1371/journal.pone.0067502 

Liu C-C. 1950. Amphibians of Western China. Fieldiana: Zoology Memoirs Volume 2. Chicago: Chicago Natural History Museum

Ogilvie MB, Choquette CJ, 1999. A Dame Full of Vim and Vigor: a Biography of Alice Middleton Boring: biologist in China. Amsterdam: Harwood.

Zheng. 2015. Alice M. Boring: a pioneer in the study of Chinese amphibians and reptiles. Protein & Cell 6, 625-627 DOI 10.1007/s13238-015-0165-1