Tuesday, 6 June 2017

How did he come to write that?

My eye, in speed reading a review of a biography of Sir Hans Sloane in The Times (Saturday 27 May), came to a sudden halt:

Sloane was no Darwinist; the flora and fauna, animals and artefacts he was to acquire articulated a vision of providential order.

Not only was there an obvious tautology describing the collection but Sloane could hardly have been a Darwinist. Sloane, whose collection formed the basis of the British Museum was born in 1660 and died in 1753. The Origin of Species was published in 1859.

I do hope the Victoria and Albert Museum has a copy of Ernst Mayr’s The Growth of Biological Thought for the author of the review is its new director, the former Labour MP, Tristram Hunt.

Komodo Dragon: extending the saliva story

The previous post generated a number of emails on the use of biologically-active substances in saliva by the Komodo Dragon to help kill its prey, ranging from ‘unnecessary and highly speculative’ to ‘generally supportive but needs more work’. I was also told that the post seemed somewhat harsh. It was not meant that way but I think my style in writing it reflects the sort of debate that has arisen and the tone adopted by some authors and commentators. The comments/replies on a paper* are as robust as any I have seen in print for a long time.

Much of the controversy centres on use of the terms ‘venom’, ‘venomous’ and ‘venom glands’. I will not go into the arguments further here but there is a long-standing problem in naming structures or molecules for presumed or first-discovered function, potential function or partial function. The names of hormones and growth factors are well-known nightmares in this regard. There are actually two hypotheses, one an evolutionary question on the stage at which reptiles acquired the capacity to produce venom—the Toxicoferon Hypothesis—and the related but distinct question of how the Komodo Dragon (and possibly other extant and extinct monitor lizards) kills its prey. This latter question is susceptible to morphological, chemical, physiological and pharmacological observation and experiment as demonstrated by Bryan Fry and his international team in their original paper. I will restrict myself to expanding the dragon story.

Typical Komodo Dragon habitat on the island of Rinca, part of the Komodo
National Park, with gullies and open areas of grassland

My own view is that there is a chain of events by which biologically active substances in saliva could be used to decrease the time between initial attack and death of the large mammal prey. At present, though, I see a gap in knowledge between a scenario which describes what could happen and one that describes what does happen. I also see it as a gap that could be filled and which, if filled, would subdue further objections and a great deal of speculation on alternative roles for biologically active substances in the Dragon’s saliva.

There is strong evidence in favour of saliva doing something—and something deleterious to the life of the prey. The presence of a relatively large lumen in the mandibular gland where secretion can be stored is highly suggestive of the use of a ready store of saliva when a dragon attacks prey, and a store that can be delivered to the base of the teeth. The authors of the original papers also showed by direct biological assays that dragon saliva has components that act to cause vasodilatation and decrease blood pressure and to contain substances that are potent anticoagulants.

Therefore, a good case has been made for local effects of biologically-active substances on the wound inflicted by the dragon—parallel deep slashes inflicted by pulling after the initial bite. Diffusion into the tissues surrounding the wound would increase the rate of blood loss and keep the severed ends of large and small arteries open and the blood flowing from all severed vessels. That’s where the relatively low bite strength of the Dragon which was demonstrated by Fry and his collaborators would be of selective advantage. If the Dragon bites, pulls what have been described as its steak-knife teeth across blood vessels (‘grip-and-rip’), and holds that grip, the last thing it needs is a strong bite. Compression by a strong bite would compress the wound and slow the rate of blood loss. Moreover, it would decrease the rate of movement of substances from the saliva away from the wound into surrounding tissues and into the circulation through venous or lymphatic drainage.

So, as far as local actions of saliva are concerned, they must be present and I can think of experiments that would test how far diffusion would take them into surrounding tissues. 

Central effects, for example, in decreasing blood pressure, would be harder but not impossible to demonstrate, as would establishing the concentrations of substances from saliva in the peripheral circulation of the prey in order to determine whether they reach the levels required to exert the effect that can be demonstrated with particular concentrations in biological assay systems. The latter is not a trivial question with substances that would be appearing in the circulation relatively slowly from a wound and which may be relatively quickly broken down into inactive compounds.

The presence of several compounds known to be part of the arsenal of toxins deployed by classic venomous reptiles adds weight to the suggestion of some systemic role for Dragon saliva in the bitten animal. Others have suggested that may may fulfil other roles in the mouth or in digestion of the prey before ingestion and the action of stomach enzymes; I do not find the latter argument compelling although it could be tested experimentally.

So, while demonstration of central toxic events has not yet been attempted, there must be a local effect of saliva, at least, on the gripped-and-ripped prey. The question that remains on this local action is whether the effect is biologically significant in shortening the life or ability to resist of the animal that has been ambushed, or is so in a sufficiently large number of attacks as to confer a selective advantage.

Both local and systemic actions rely on getting saliva into the wound. Different durations of bites could have different effects. The mandibular gland implicated in storage seems to work in a similar way to that of back-fanged snakes in that the pressure exerted by chewing forces the secretion out. If that is so then a ‘grip-and-rip’ feeding attack could have an entirely different outcome from a quick offensive or defensive nip.

Some commentators have suggested testing the components of Dragon saliva on their natural prey. However, what is their natural prey? Water Buffalo were introduced relatively recently, Timor Deer in antiquity while domestic goats are, well, domestic. The Komodo Dragon and its extinct relatives appear to have been around the Indonesian islands, where they spread from Australia, even before the now extinct dwarf elephant appeared in their habitat so that fundamental mismatch between the bulk and apparent adaptations for killing large animals of Komodo Dragons and the size of potential prey species seems to be unexplained.

Other questions arise like are there differences between the sexes in the size of prey and feeding strategies, adult females being lighter than males? Do juvenile Dragons attack prey that is larger than that attempted by, say, Water Monitors (Varanus salvator) of similar size and, if so, would that make the use of saliva as a chemical weapon to help in subduing prey more likely? In other words, the advantage may come more to juveniles tackling large prey than to adults. Indeed, if other species such as the Lace Monitor or Goanna (Varanus varius) from Australia have a similar array of potential biological agents, which seems to be the case, and in quantitatively equivalent amounts, might the whole arrangement be an adaptation to extend in size the range of prey that can be killed and eaten by some or all monitor lizards?

So, after arguing with myself several times and learning lots about venomous and non-venomous reptiles, that’s may take on the Komodo Dragon’s feeding method in the light of present evidence. In essence, I argue that the available evidence points to a local chemical role for saliva in helping to subdue/kill large prey (while recognising that sheer physical force may often or sometimes be sufficient). As for toxins in saliva having a systemic effect on the prey, I argue that the gap between the prima facie potential effect and actual effect has not yet been filled by experimental data. And as to whether we should call Dragons ‘venomous’ or the gland the ‘venom’ gland…

...I will leave to others.

Whatever the final outcome on these fascinating and enigmatic lizards, the authors of the 2009 paper have done a signal service in examining how it and other extinct and extant monitor lizards kill their prey and have not shied from erecting hypotheses on possible mechanisms and their wider importance in the evolution of reptiles. 

*Fry BG, Casewell NR, W├╝ster W, Vidal N, Young B, Jackson TNW. 2012. The structural and functional diversification of the Toxicofera reptile venom system. Toxicon 60, 434-448. Weinstein SA, Keyler DE, White J. 2012. Replies to Fry et al. (Toxicon 2012, 60/4 434-448). Part A. Analyses of squamate reptile oral glands and their products: A call for caution in formal assignment of terminology designating biological function, Toxicon 60, 954-963. Kardong KV. 2013. Replies to Fry et al. (Toxicon 2012 60/4 434-448). Part B. Properties and biological roles of squamate oral products: The “venomous lifestyle” and preadaptation, Toxicon 63, 113-115. Jackson TNW, Casewell NR, Fry BG. 2013. Response to “Replies to Fry et al. (Toxicon 2012, 60/4, 434–448). Part A. Analyses of squamate reptile oral glands and their products: A call for caution in formal assignment of terminology designating biological function”, Toxicon 64, 106-112. Weinstein SA, White J, Keyler DE, Kardong KV. 2013. Response to Jackson et al. (2012), Toxicon 64, 116-127.

Saturday, 20 May 2017

Komodo Dragons. A peaceful morning in the Komodo National Park and an acrimonious debate on reptilian venoms

Last September’s Expedition Cruise from Darwin through the Lesser Sunda islands of East Timor and Indonesia included stops at Rinca and Komodo. Ever since my fourth cousin once removed visited Komodo in 1956 I have wanted to see Komodo Dragons alive and in their natural habitat. They did not disappoint. We saw very large males (hanging out around the kitchen of the ranger station on Rinca hoping for a hand out), females and juveniles (but not the hatchlings which apparently take to the trees to avoid their predatory parents). One female was digging out the nest mound of a megapode, the Orange-footed Scrubfowl (Megapodius reinwardt) in which to lay her own eggs, September being the egg-laying time in their breeding cycle.

When we got back I had a chance to look at and think about the various hypotheses that have been advanced as to how Komodo Dragons—and, possibly, some other monitor lizards—kill their prey. The highly publicised but never properly tested proposal that Komodo Dragons are venomous in the sense that venomous snakes are venomous, i.e. toxins delivered by injection having a very or fairly rapid systemic effect on the prey, seems to be in the process of being discarded in the course of some pretty acrimonious arguments, along with the associated hypothesis of a single, early origin of venom in reptilian evolution—the Toxicofera hypothesis. The other idea, that pathogenic bacteria harboured in the mouth of dragons causes sepsis in prey animals that are bitten but escape the initial attack, doesn’t seem that convincing or special given the likelihood of infection from a bite from any animal, as any postman will testify, especially if that postman were to immerse his bitten ankle in fetid water, as non-native water buffalo do when bitten by a Dragon. If I were to bite a Timor Deer on the leg, there is every likelihood an infected wound that could impede mobility would ensue. 

Given the opposition to the Toxicofera hypothesis and the contentious nature of the evidence for Komodo Dragons being venomous, it seems a pity that the BBC repeated last November the screening of an episode from its 2011-12 season of the Natural World Series called Komodo—Secrets of the Dragon that was devoted virtually entirely to that proposition and its main protagonist. Had this been a programme about a topic other than science-led natural history the BBC would have been falling over itself to show someone with the opposite view, however perverse. As it is, the viewing public in Britain has been left with the impression that the venomous nature of the Dragon is accepted. At the very least the BBC should have been aware of what was going on (by reading Wikipedia for example) and before rescreening it should have added an annex to the original programme. That annex could have  explained the opposing views and evidence—some of which made news media reports*—that have been accumulating since 2009. Adam Hargreaves (Oxford), Abigail Tucker (King’s, London) and John Mulley (Bangor), who produced a devastating critique** of the toxicoferan hypothesis in 2015, should have been consulted and involved. But let’s leave the BBC and its usually excellent (but sometimes spectacularly poor) natural history programmes and return to the mouth of the dragon.

None of the criticisms of the venom hypothesis imply that the composition and quantity of saliva are not of selective advantage to the despatch of prey, subsequent swallowing and digestion or protection of the oral cavity against infection. Nor, indeed, do they refute the idea or evidence that saliva may have local beneficial—to the Dragon—effects on inflicted wounds, like the application of a secreted anticoagulant, for example.

The drooling mouths of some of the male Dragons we saw were impressive. The only comparable example I could think of was my late mother-in-law’s Boxer dogs given the slightest hint of finding something edible. With no obvious sign of food or feeding activity, is Dragon saliva being used for some other purpose like scent marking?

The accumulated data that I have found suggests to me that Komodo Dragons, as originally thought, kill their prey by sheer brute force from wounds inflicted by a very large mouth with very big teeth. In one study†, 17 attacks on large prey were observed, 12 were fatal. Of the 5 that escaped with injuries to their limbs and rump, 1 was quickly attacked and killed by a second Dragon, 2 died within hours, one fled being pursued by other Dragons and one limped away without being pursued. The eventual fate of the two that possibly survived is not known.

One may though ask how, if the Komodo Dragon originally preyed upon the now extinct dwarf elephant, Stegodon, of Flores, as suggested in 1987 by Jared Diamond, those beasts (smaller than a domestic water buffalo) were killed? Would biologically-active substances in saliva have been of selective advantage?

Nowhere have I found (but I am not have looked in the right place) any discussion of the selective benefits of a slow death of the prey to the predator. A snake with a fast-acting neurotoxin can quickly track and swallow its prey without that investment in metabolically expensive venom being lost to another snake or any old predator happening to find the corpse. But let’s say a Dragon does inject toxins with a small bite and the animal runs away to die. There is no guarantee that the investment in venom would pay off. With lots of other Dragons around, the prey could be lost entirely or the original killer would get only a small share in a communal but competitive feeding session. Surely, if monitor lizards are venomous at all then why have they not evolved a more effective venom to ensure a quick kill?

The venomous dragon and other monitor lizards hypothesis has been around now for ten years. I find it sad that so little has been done at the whole animal and tissue levels to test it. I found some of the original observations and experiments‡ unconvincing. But given the captive populations of Dragons and a local abundance on Komodo and Rinca, a rigorous examination of the whole question cannot be beyond the bounds of practical realisation or funding.

*e.g. Zimmer C. 2009. Chemicals in Dragon’s Glands Stir Venom Debate. New York Times, 18 May 2009. Yong E. 2015. A Venomous Fight Among Reptile Scientists. The Atlantic, 2 November 2015

*Hargreaves AD, Tucker, AS, Mulley JF. 2015. A critique of the toxicoferan hypothesis. In, Gopalakrishnakone P (ed), Malhotra M (ed). A critique of the toxicoferan hypothesis. In Evolution of Venomous Animals and Their Toxins: Toxicology. Springer Netherlands, p 1-15. DOI: 10.1007/978-94-007-6727-0_4-1

†Bull JJ, Jessop TS, Whiteley M. 2010. Deathly drool: evolutionary and ecological basis of septic bacteria in Komodo Dragon mouths. PLoS ONE 5(6): e11097. doi:10.1371/journal.pone.0011097

‡Fry BG Wroec S, Teeuwisse W, van Osch MJP, Moreno K, Ingle J, McHenry C, Ferrara T, Clausen P, Scheib H, Winter KL, Greisman L., Roelants K, van der Weer L, Clemente CJ, Giannakis E, Hodgson WC, Luz S, Martelli P, Krishnasamy K, Kochva E, Kwok H, Scanlon D, Karas J, Citron DM, Goldstein EJC, Mcnaughtan JE, Norman JA. 2009. A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus. Proceedings of the National Academy of Sciences of the USA 106, 8969-8974 doi 10.1073 pnas.0810883106

Monday, 8 May 2017

Burkhardt and Vevers: Family Links in the Early 20th Century

Late last year James Ritchie contacted me after reading my articles on Colonel Valentine Burkhardt (12 April 2016) and Dr Gwynne Vevers (4 October 2016) in order to point out that members of the two families were close friends in the years before the First World War.

I was fascinated to read your article on Val Burkhardt—he was my grandmother's cousin. My grandmother's mother, Marie-Beatrice Siordet (nee Caldwell) was the younger sister of Annie Claudia, Val Burkhardt’s mother. Thank you for your research which has greatly expanded my knowledge of this interesting man. I also note that you have written about Gwynne Vevers and I wondered if you knew of the link between the Vevers family and the Burkhardts?  It is through my great uncle Gerald Caldwell Siordet. Briefly, Siordet was at Clifton College with his cousin Val and then went up to Balliol where he met and became great friends with the Herefordshire artist Brian Hatton. After Oxford, Hatton and Siordet shared a studio in South Kensington. Gwynne's father Geoffrey Vevers [1890-1970] was a medical student and a cousin of Hatton (their mothers were sisters) and the three of them socialised in London just prior to the first war. Hatton and Siordet were subsequently killed in the war. Val B visited the site of Hatton’s death in Egypt and wrote to Siordet about it.

More details can be found in the book by the late Celia Davies, Brian Hatton. A Biography of the Artist (1887-1916) published by Terence Dalton in 1978. However, the book is worth reading for more than those details. It is a fascinating account of Hatton’s early years and his development as an artist. It is as enjoyable and informative of life in Britain the thirty years up to the First World War as Gwen Raverat’s Period Piece.

Brian Hatton was killed on 23 April 1916 in the Battle of Katia, 25 miles east of the Suez Canal. Fifty Royal Engineers, plus a detachment of Worcestershire Yeomanry 180 strong sent to guard them, were sinking a well when they were attacked by 2-3000 Turkish infantry who came across them. He left a wife and baby daughter.

Gerald Siordet was in France when he heard the news. He then wrote to his cousin Val to ask for any more information since Burkhardt was then serving in Egypt. The then Captain Burkhardt replied on 27 September 1916. In the reply (the full text is in the book) Burkhardt stated that he was having a better memorial than the few sticks  and the bottom of a biscuit tin bearing an illegible inscription he found including a separate one for ‘2 Lieut Brian Hatton Worcester Yeo, A fine artist and a gallant soldier’. In a footnote to the letter, Celia Davies noted that after the war the Yeomen were reburied at Kantara on the Suez Canal.

Gerald Caldwell Siordet, artist, poet, critic and one-time tutor to Aldous Huxley was awarded the Military Cross for conspicuous gallantry on the Somme in 1916. He was killed on 9 February 1917 leading an attack on a Turkish position in Mesopotamia (now Iraq); his body has never been found. Val Burkhardt’s letter to him had ended: ‘I hope you are not for Mes[o]pot[amia]’.

Brian Hatton in his London studio (from here)
Gerald 'Jack' Caldwell Sioret (from here)
Geoffrey Marr Vevers (1890-1970) when Superintendent,
London Zoo
(Animal & Zoo Magazine December 1938)

Friday, 31 March 2017

The butterfly’s tongue and the steel rule

‘Why is that there?’, said my four-year old grandson in an accusatory tone when he spotted a Stanley coiled flexible steel rule on my desk. ‘Ah, I need to take a photograph of it to show how a butterfly’s tongue works’, I replied. A look of utter puzzlement and then of disdain on the boy’s face demonstrated his certain knowledge of having a silly grandfather.

L.E.S. Eastham
My wish to illustrate this post with a steel rule was occasioned by a jolt of memory when I was writing a previous one on BEPS—The Invertebrata by Borradaile, Eastham, Potts and Saunders. I had a vivid recollection of the words being said, but not of the face behind the words, during a lecture at Sheffield on insects that in the old days (i.e. before 1958 when Eastham retired as Professor of Zoology) we would have had to have known how the butterfly proboscis works since he, Eastham, it was who worked it out. However, the lecturer added that the only thing about the mechanism that one had to remember was that it works like a steel rule. The more I thought about who the lecturer was, I have the vague notion that it was the Sheffield born-and-bred—and educated—Fred Segrove (1911-2003).

Having remembered nothing else about the butterfly proboscis, I recently found the original paper by Eastham and Eassa, published in 1955 when Eastham was 62. It is a highly impressive and long paper and involved making serial sections and some physiological studies. It demolished previous theories on how the proboscis worked. Eastham himself provided a short explanation in the later editions of BEPS:

The adults live on the nectar of flowers, and to absorb this a highly specialized proboscis has been formed from the greatly elongated galeae of the maxillae, each being grooved along its inner face and locked to its neighbour…Each half of the proboscis is a tube in itself into which passes blood from the head, and also a trachea and a nerve. Across the cavity of this tube there pass a number of oblique muscles. At rest the proboscis is tightly coiled like a clock spring under the head. When feeding the proboscis is extended and its tip placed in the food source. It is now recognized that the elastic properties of the cuticular wall of the proboscis account for the coiled condition when resting. Extension of the proboscis is brought about by the internal oblique muscle of each galea. These, working in conjunction with a stipital valve controlling the closure of the passage between cephalic and galea haemocoeles, cause the proboscis to develop a dorsal keel along its whole length. The attainment and retention of this new shape depends on the turgidity of the galea tube and the elasticity and flexibility of parts of the cuticular wall. For mechanical reasons it cannot in the keeled position be retained in the coiled state and extension of the proboscis results.In feeding, a complex pharyngeal muscular apparatus causes the fluid food to be sucked into the mouth. The length of the proboscis in many cases corresponds to the depth of the corolla of the flower which the species frequents, and in the Sphingidae (hawk moths) may be greater than that of the body…

In Eastham’s chapter in BEPS there is though no mention of the analogy of a retractable, flexible steel rule, which was used in the original paper and in which a Mr F.W. Adams was thanked for thinking of it:

…a coiled steel rule, when coiled in its case, is flat in section, but when it is drawn out it assumes a curved transverse section, convex on one side and concave on the other, and in this state attains a condition of extension. In this case the rule has to be forced into its case, and bending can only occur when its transverse curvature is flattened out. The condition of rest is one of extension and force has to be applied to coil it up, the rule having been manufactured with these properties.

The difference between a steel rule and a butterfly’s proboscis is, of course, that it is muscular action which produces the curved transverse section for extension and elasticity which returns it to a flat cross section after the muscles relax and thence its recoil.

Small Tortoiseshell with proboscis coiled

Comma feeding with proboscis extended. Eastham & Eassa also explained
how the 'knee-bend' in the proboscis was formed

There is an statement in the paper which sixty-odd years after it was written I find odd:

…As a result of complete analysis of these structures, of observations on the animal during feeding—of numerous operations involving nerve sections and perforations of the haemocoele—a new theory is offered on the proboscis mechanism for which the senior author (L.E.S.E[astham]) alone is responsible.

I can think of several explanations for this statement. Did Eassa disagree is one. Did Eastham think that if the new theory were to be shot down in flames, he was making sure that Eassa could not be blamed? But then the paper was sent to the Royal Society for publication by V.B. Wigglesworth, the name in insect physiology in the 20th Century; he must have been sufficiently impressed. There remains the possibly unworthy thought that Eastham was making sure he got the credit but that goes against Eastham’s reputation in Sheffield amongst those who had worked in his department like E.T.B. Francis, F. Segrove and J.D. Jones as a gentlemanly, paternal figure. And what had Eastham to gain at the age of 62 and three years from retirement? The only possibility is that he was, and perhaps for the last possible time, up for election to the Royal Society. He, like all the other authors of BEPS, was not elected but I do not know—and cannot know until the archives for that period are opened—if he was ever proposed.

But what of Eassa? Who was he, what was he doing in Sheffield and what happened to him?

Youseff Ezeddin Eassa (1914-99) was a famous Egyptian author as well as being Professor of Zoology at the University of Alexandria. There is a website devoted to him and his work. He was a graduate of the University of Cairo and is shown as arriving in Sheffield in 1948 as a Ph.D. student but also as an established playwright and author. However, his Ph.D. thesis (A contribution to the postembryonic development of the head of Pieris brassicae (Linn)) is dated 1949 so he may have travelled to Sheffield earlier than 1948. He must have stayed in Sheffield for some time after 1949 because the Eastham & Eassa paper was sent to the Royal Society in April 1954 and no new address for Eassa is shown.

While in Sheffield he wrote stories and plays that were broadcast on BBC radio. He recalled that his favourite companion at coffee was Hans Krebs, later Sir Hans and then Professor Biochemistry at Sheffield. Eassa was a Fulbright Fellow in Berkeley and Illinois in 1960-61.

Youseff Ezeddin Eassa (from here)

I hope I get the opportunity of explaining to my grandchildren not only how the butterfly feeds, using, of course, the steel rule as an aid, but also of making sure they know that international scientific collaboration was not invented by the EU (as some young academics in Britain clearly believe) and that academics could meet and exchange ideas in university staff (faculty for readers more familiar with the U.S. university system) clubs rather than remain ensiled, as appears to be the case at present, in departmental comfort zones.

Oh, and here is the rule:

Eastham LES, Eassa YEE. 1955. The feeding mechanism of the butterfly Pieris brassicae L. Philosophical Transactions of the Royal Society B 239, 1-43.

Thursday, 30 March 2017

The University of Hong Kong was a site for more than birds in the 1960s

In the 1960s, the University Compound’s pathways teemed at night with the toad, Duttaphrynus melanostictus (formerly Bufo melanostictus), along with introduced Giant African Snail, Achatina fulica.

Duttaphyrnus melanostictus

The lily pond had large numbers of Guenther’s Frogs (Sylvirana, previously Hylarana guentheri).

Lily pond, University of Hong Kong, constructed in the early 1950s. The trees

were non-native. From Mellor, B. The University of Hong Kong, An Informal
History.  Hong Kong University Press, 1980

After heavy rain, the gardeners disturbed a couple of the microhylid, Kaloula pulchra, outside our lab building, the old Building 15 of the medical school (which by 1965 had moved to its new quarters on Sassoon Road).

Kaloula pulchra

The same location revealed a couple of Brahminy Blind Snakes under an old flowerpot. This species, now going under the name of Indotyphlops braminus, has been introduced into many parts of the world in...flowerpots.

This photograph from 1950 shows a University Congregation processing along
Pokfulam Road. I found Kaloula pulchra over the wall to the right, 17 years later
All the building in view have been demolished. From Mellor 1980

Street lamps and flats had the Oriental Leaf-toed Gecko, Hemidactylus bowringii. They often looked thin and underfed like the one I photographed.

Hemidactylus bowringii

A squad of gardeners looked after the compound and cleared fallen leaves. Snakes were, therefore, not to be expected. However, we did one spot a couple of times an Indo-Chinese Rat Snake, Ptyas korros, on the ground at the base of a tree directly below our balcony at 3 University Drive.

The only other snake seen took me by surprise. I opened a lab drawer containing glassware one morning to find a White-spotted Slug Snake (Pareas margaritophorus) less than happy at being disturbed.

If only digital camera traps had been invented in the 60s, we might have got an idea what, if any, mammals, other than rats, mice and domestic cats and watchmen were living in or visiting the Compound. A Chinese Ferret Badger (Melogale moschata) or two would be my bet.

Oliver LA, Prendini E, Kraus F, Raxworthy CJ. 2015. Systematics and biogeography of the Hylarana frog (Anura: Ranidae) radiation across tropical Australasia, Southeast Asia, and Africa. Molecular Phylogenetics and Evolution 90, 176-192. http://dx.doi.org/10.1016/j.ympev.2015.05.001 

Hedges SB, Marion AB, Lipp KM, Marin J, Vidal N.  2014. A taxonomic framework for typhlopid snakes from the Caribbean and other regions (Reptilia, Squamata). Caribbean Herpetology 49, 1–61.

Tuesday, 28 March 2017

Why was the University of Hong Kong a good site for birdwatchers in the 1960s?

In the early bird reports for Hong Kong, the University Compound (now called ‘campus’) often got a mention. There are two reasons. The first is that from Herklots in the 1930s there was often a birdwatcher or two living and working there. The second is that it was wooded hillside interspersed with green spaces, shrubberies, ponds and gardens. Some of the trees, unlike the wooden floors, window frames and roof timbers of the buildings, may have survived the Japanese occupation. The steep paths and steps (84 between the old Building 15 and 3 University Drive) allowed views into the tree tops.

1965 view from 3 University Drive over part of the University Compound.
The white buildings are on the north side of Pokfulam Road.
The partially hidden brick buildings were pre-clinical labs
vacated when the medical school moved to Sassoon Road

The compound was though already falling from grace in the early 1960s because of the spate of new building from the early 1950s (new staff flats) until the, for then, large new chemistry block, library, students’ union and first phase of Robert Black College. However, from 1965 until we left in 1968, the compound was undisturbed by new building.

The Compound. bounded by a nullah to the west. was a good place to see all the common Hong Kong birds including winter and summer visitors. It was also good for passage migrants (the delights of Po Toi island were then unknown). Blue and White Flycatchers appeared in numbers in April 1966. What are again named Ince’s or Chinese Paradise Flycatchers again (after a period of being lumped into Asian) appeared in the spring. We saw a spectacular fully-tailed male each day from 12 March until 5 April 1966.

Above the university and to the west of University Drive (now, I see renamed University Avenue), Conduit Path was good in the winter for thrushes and Rubythroats and the Violet Whistling Thrush was rarely absent from the sides of the nullah that, further downhill, bordered the Compound.

We overlooked the tree tops in the western part of the compound when we lived for a year in a flat in the very well designed 3 University Drive (now demolished). Cicadas in the evenings and bulbuls  by day were the overwhelming sounds. All could be heard because traffic on Pokfulam Road was relatively light. Large insects flew on to the balcony in the evenings, once pursued by a Collared Scops Owl that did a quick about turn when it saw me.

However, the green and pleasant old Compound did not last. High-rise building followed high-rise building as student numbers increased. Departments housed on the north side of Pokfulam Road were moved into the Compound as the buildings were demolished for road widening. The old preclinical medical buildings were cleared and huge blocks replaced the gardens.

Writing in 1983 in what was then the University’s newspaper, Interflow (Issue 39, March 1983), the late Harry Edie, a botanist, questioned what was going on under the self-explanatory title, 'Tropical Paradise or Concrete Inferno'. In making a plea for expert botanical input into planning the campus in order to preserve wildlife and continue to provide amenity value to the human inhabitants surrounded by closely packed tall buildings, Harry showed photographs of the Compound as it was in the 1970s.

One of Harry Edie's photographs showing the University Compound in
the 1960s and early 1970s
Another Harry Edie photograph showing the (non-university) hillside
in the foreground. No 3 University Drive is front central; No 2 is the
orange block. Robert Black College has the blue roof. The Vice-
Chancellor's Lodge is on the far left. The large block of flats is beyond
the University Compound.
Photograph of 3 University Drive from Harry Edie's article. Note the
lush vegetation of the gardens
1966 view from Conduit Path. The University Library is left; 3 University
Drive is front centre and the old house on University Path is right.
All now demolished except the library

The general sub-tropical regrowth of trees and plants incorporated into landscape designs did mean that in the 1990s the Compound was still a good habitat for birds, even though much of the land area was covered by concrete. Between the 1960s and 1990s a number of species expanded their ranges. For example, apart from isolated reports the only reliable site for Fork-tailed Sunbirds in the mid-1960s was Tai Po Kau Forest Reserve in the New Territories. By 1997, a pair was nesting in creeper at Robert Black College a short distance from our room.

Further expansion of the University, this time with blocks built to the west of the old Compound has completely altered the landscape in the past fifteen years. But some of the old trees and wilder areas remain and new planting around the buildings can be seen. It is difficult to assess by occasional visits at different times of year whether the Compound, sorry Campus, still provides a stop-over for passage migrants or suitable habitat for the common residents and seasonal visitors.

The Hong Kong Birdwatching Society no longer lists the University as a good site but it does include the land above it—Lung Fu Shan.

Tuesday, 21 March 2017

A revision of an iconic textbook on invertebrates—the famous ‘BEPS’—was panned by a reviewer in 1958

It is hard to imagine that one of the advanced textbooks which you only got your hands on in the VIth form and which lived with you until the end of an undergraduate course in zoology took a pasting from a reviewer for New Scientist

The mention of ‘BEPS’, as the book was known throughout the world often brought forth the chant of its authors as a sort of mediaeval religious incantation: Borradaile...Eastham.....Potts.......and Saunders*.

This is what the review (New Scientist 17 July 1958) of the third edition said:

The Invertebrata. A manual for the use of students. By L. A. Borradaile, F.A. Potts, L. E. S. Eastham and J. T. Saunders. 3rd Edition revised by G. A. Kerkut. (Cambridge University 
Press, 795 pp., 55s.) 
BEPS has been the standard English text-book on invertebrate animals for twenty-five years, and will be familiar to anyone who has taken even the briefest University course in zoology. It is a fact book for undergraduates, for more senior zoologists in search of their memories, and for sixth-form libraries This new edition will maintain, but not enhance, its reputation as a useful but dull book. Of the four original Cambridge authors, only one. Professor Eastham, has been in a position to revise his part, and the whole has been undertaken by Dr. G. A. Kerkut, of Southampton. 
     The changes in the text are not large, and much of the increase of seventy pages is due to the addition of a useful appendix on zoological literature and to an increase in the number of illustrations. The text has been broken up into a series of paragraphs with sub-headings. which gives a somewhat staccato effect to the whole. Many errors of fact have come through unaltered, as have many general passages which were badly in need of reshaping in the light of new information. Some of the alterations have been made necessary by changes or expansions in the classifications used. Some of these are for the better, some for the worse; but the reader is now given a minimum of 400 group names to be learnt, in place of 280. 
     The earlier editions left out a few small groups. Some of these have now been included, but others are still ignored. For example, Kinorhyncha and Priapulida now appear, but Mesozoa and Symphyla, both of which are of more interest, are absent. 
     Most of the old and excellent illustrations reappear, and these have been improved by transferring the names of structures illustrated from the captions to the guide lines. But they are supplemented by new drawings, and some of the old ones have been redrawn. Manyof these arc technically execrable and some banal in content as well. A comparison of Figure 218 in the second edition with Figure 226 in the new will illustrate both these faults. 
     Revision of a standard text-book is an onerous task which no one would undertake lightly, and, where the textbook is one that will be largely used by students, its publishers must carry considerable responsibility. This one falls short of what is to be expected of so distinguished a house. 
R. B. Freeman.

[Richard Broke Freeman (1915-1986) was Reader in Taxonomy at University College London although he is probably best remembered as a bibliographer and expert on Charles Darwin.]

The first edition of BEPS was published in 1932 By 1958 two of the original authors (Lancelot Alexander Borradaile 1872-1945; Frank Armitage Potts 1882-1937) were dead. John Tennant Saunders 1888-1965 (grandfather of Jennifer Saunders the comedian and actress) had recently retired as Principal of University College, Ibadan, Nigeria. Leonard Ernest Sydney Eastham (1893-1977) was about to retire from the chair of zoology at Sheffield but revised his section on insects. Gerald Allan Kerkut (1927-2004) was responsible for the revision of the third and fourth editions; it was not his last book to be panned by a reviewer.

Was the poor reception of the third edition of BEPS in 1958 the reason why a fourth appeared in 1961?

What I think this rather sad tale for the original BEPS quartet means is that textbooks do not age well. The whole style and treatment makes revision beyond a certain point difficult especially in such a wide-ranging book by a single author. BEPS was essentially a 1920s book hanging on into the 1960s. As fashions changed and as soon as an alternative appeared, in the form of Invertebrate Zoology by R.D. Barnes (Saunders, 1963), it was dropped. However, BEPS is still a good starting point for looking things up—if only I could find my copy.

L.A. Borradaile
F.A. Potts (from here)
L.E.S. Eastham (from here)

...and I cannot find a photograph of J.T. Saunders.

*The order of the authors is BEPS on the jacket and BPES on the title page, Eastham and Saunders being described as having ‘chapters by’.

Friday, 17 March 2017

Teddy Bears and Hamsters: A 1900s Pet Scam

Still on the European Hamster (Cricetus cricetus), I came across this story in The Zoo Story by L.R. Brightwell, a history of London Zoo published in 1952.

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

In his chapter covering the decade 1901-1910 and under the heading of one of his drawings showing how Fellows of the Zoological Society were dressed at the time while looking at a far more intelligent Chimpanzee, he wrote on the appearance of a new toy:
     …A matter of unscientific interest also was the arrival from U.S.A. of that still popular nursery potentate, the Teddy Bear…It is now generally agreed that the toy was really inspired by the Koala, or Billy Blue Gum, an Australian marsupial. But we are all full of Teddy Roosevelt, his famous range of dentures, fire-eating speeches and highly coloured hunting adventures. Whatever the nursery favourite's real origin, it is from the irrepressible "he-man" president that it took its name. The toy's immediate and tumultuous popularity led to a strange development in the animal trade. Certain livestock dealers—with a shrewd eye for what the public evidently wanted—gave it the "Teddy Bear Rat". This was the hamster, a chubby, handsomely marked beast not unlike a guinea pig and so abundant in some parts of the Continent as to be a plague. This is the rodent said to have eaten the cruel bishop in the Rhenish “Mouse Tower". To launch such a dirt-cheap creature on the public at an extravagant figure seemed to the business mind elementary common sense. But the hamster unfortunately combines with the guinea pig's chisel teeth a very unguinea-pig-like temperament. It led to so many complaints and damaged fingers that the police eventually prohibited its sale. The Zoo soon had to refuse offers of Teddy bear rats, so eager were disgruntled householders to part with their spiteful pets.

The European Hamster has always had a terrible reputation for biting its keepers in captivity and for defending itself in the wild. George Jennison in his Natural History Animals of 1927 wrote:
     It is an irascible creature, a bold and determined fighter with its own kind and against vultures and smaller birds, dogs, cats and the lesser carnivores that prey upon it.

The UFAW Handbook 6th edition says European hamsters are capable of inflicting serious bites but that at the Hannover medical school they have been tamed by frequent handling and personal attention to individuals such that ‘a large degree of tameness can be achieved in successive generations’. That is also true of the other hamsters kept as pets and in labs, the Syrian, Chinese and Djungarian but the European is that much bigger and a braver (wo)man than me would be needed to start the process.

European Hamsters and Maize Fields. A Nutritional Route to Local Extinction?

I have not seen a European Hamster (Cricetus cricetus) in the wild despite having twice looked for them at dusk in a hedgerow in Hungary where they had previously been seen—a classic case of, ‘if only you had been here last week’.

In the west of its range, notably in France, the hamster has declined markedly over the past decades. All sorts of reasons have been suggested, most to do with changes in agriculture. A recent paper1 by Mathilde Tissier, Yves Handrich, Odeline Dallongeville, Jean-Patrice Robin and Caroline Haboldfrom of the University of Strasbourg has suggested a nutritional reason for that decline. Previously members of that team had found an association between the decline of the species in France, where it was common on agricultural land, and the increase in the growing of maize by farmers2.

Observations of the hamster in the wild have indicated they feed on cereal crops, tubers and invertebrates. Hamsters hoard large amounts of food in their burrows and they hibernate. There is evidence that after hibernation female hamsters do not emerge from their burrows before their first pregnancy of the season, relying until then on their hoarded seeds. During gestation and lactation they emerge and supplement their diet of seeds with fresh plants like clover and invertebrates such as earthworms.

Using females from a captive colony of European Hamsters, the group first studied the effect of four different diets after emergence from hibernation: wheat+clover; wheat+earthworms; maize+clover; maize+earthworms. Similar numbers of young were born with all four diets. However, there was a marked difference in their early survival. On the wheat+earthworm diet, 80% of young survived to weaning while on the other three diets survival to weaning was under 12%. Clearly, something was missing from the diet; protein at about 18% of the diet one would guess with the clover supplement (compared with over 40% with earthworms). However, there was a clear difference between wheat and maize in terms of survival of the young.

At this point, human nutritionists would be bouncing up and down to tell you that there is a key difference between wheat and maize: the content and bioavailability of niacin (Vitamin B3 or nicotinamide) are much lower in maize and that, given the supply of earthworms rich in other nutrients that are relatively low in maize, the most likely nutrient lacking would be niacin.

The next season, a simple experiment was done. The maize+earthworm diet was compared with the same to which niacin was added. The results were clear. From a mean of less than two surviving until weaning with the maize+earthworm diet, supplementation with niacin increased that survival to over four.

The authors continued:

…regarding the European hamster, given that wild populations of this species are surrounded by 55–80% of intensively managed maize monoculture in Alsace (France), with sized field of 1.4 ha that corresponds to seven times the home range of a female, extremely low crop rotations (i.e. sometimes more than seven successive years of maize cultivated in the same plot) and high use of herbicides—dramatically reducing the proportion of adventive species—wild hamsters are undoubtedly constrained in their diet.

Now, you may ask, having demonstrated that nutritional deficiency can affect the survival of young hamsters to weaning, do the authors have any evidence that is a key cause of the decline of the species in France? In other words, do observations in the wild show the number of young emerging from the burrow, particularly from the first litter of the season, to be low?

The discursive paper (some of the data presented are irrelevant to the main story) which could have benefitted from a benignly dictatorial editor, raises several other questions. For example, nowhere I can see is any comparison made with data from the captive colony fed a presumably ‘complete’ diet. What was the litter size, survival to weaning etc. compared with the best performing experimental groups?

I must admit to being confused on the ‘normal’ litter size at birth of the European Hamster which is why a comparison with the breeding colony would have been informative. I have found value of 4-18 young, with numbers declining since about 19803. I have also found an account that there is a strong genetic element determining litter size in captive colonies4.

The reduction in litter size after parturition seemed to vary from a gradual loss on the wheat+clover diet, for example, to a complete lack of lack of maternal care in most of the animals on maize+clover. It is well known that if nutrition is inadequate or other environmental conditions are not right, female rodents kill and eat their young thereby conserving their resources to try again when the chances of producing fit young are better. Indeed a great deal of effort in he past went into devising diets for laboratory rodents, including hamsters, of course, to overcome such problems. So to those of us who have kept rodents the lack of maternal care in the malnourished hamsters was to be expected. However, true to form that British comic which masquerades as a newspaper, the Daily Mail, was on form when it picked up this story:

There is evidence in Syrian Hamsters that the sex ratio is manipulated after parturition by maternal cannibalism in different environmental conditions5. Having some proprietorial interest in mechanisms controlling the sex ratio in rodents, in my case the selective reabsorption of embryos in the Guinea Pig6, it would be of interest to know the sex ratio of the young surviving to weaning in the different experimental groups.

Again back in the real world, how many animals could be affected by niacin-deficiency from eating cultivated maize as a staple in the wild, Tissier et al. wondered. American Black Bears with young, as opposed to bears without young, avoid eating maize and other cultivated crops. They also suggested that bees could be adversely affected by feeding too heavily on maize pollen.


1 Tissier ML, Handrich Y, Dallongeville O, Robin J-P, Habold C. 2017 Diets derived from maize monoculture cause maternal infanticides in the endangered European hamster due to a vitamin B3 deficiency. Proc. R. Soc. B 284, 20162168. http://dx.doi.org/10.1098/rspb.2016.2168

2 Tissier ML, Handrich Y, Dallongeville O, Robin J-P, Weitten M, Pevet P, Kourkgy C, Habold C. 2016. How maize monoculture and increasing winter rainfall have brought the hibernating European hamster to the verge of extinction. Scientific Reports 6 25531 doi: 10.1038/srep25531

3 Surov A, Banaszek A, Bogomolov P, Feoktistova N, Monecke S. 2016. Dramatic global decrease in the range and the reproduction rate of European hamsters Cricetus cricetus. Endangered Species Research 31, 119-145 doi 10.3354/esr00749

4 La Haye MJJ, Koelwijn HP, Siepel H, Verwimp N, Windig JJ. 2012. Genetic rescue and the increase of litter size in the recovery breeding program of the common hamster (Cricetus cricetus) in the Netherlands. Relatedness, inbreeding and heritability of litter size in a breeding program of an endangered rodent. Hereditas 149, 207-216

5 Beer AK, Zucker I. 2012. Sex ratio adjustment by sex-specific maternal cannibalism in hamsters. Physiology & Behavior 107, 271-276 doi: 10.1016/jphysbeh.2012.09.001

6 Peaker M, Taylor, E. 1996. Sex ratio and litter size in the guineapig. Journal of Reproduction and Fertility 108, 63-67