Edward Bles. Part 4. Cambridge: Olms and Paul Kammerer

At the end of April 1923, 12 Madingley Road had a house guest. Edward and Bertha Bles were entertaining Paul Kammerer who had been invited to give a talk to the Cambridge Natural History Society about his claims on the inheritance of acquired characteristics. Bles and Kammerer would have had much to talk about since both kept and bred amphibians, and three of Kammerer’s claims centred on such species, the Midwife Toad (Alytes obstetricans), the Fire Salamander (Salamandra salamandra) and, to a certain extent, the Olm (Proteus anguinus).

The lecture at Cambridge provided the opportunity for a verbal punch-up between the neo-Darwinists and the neo-Lamarckians. Discussion at the time was concerned with the possibility that the scientific world was being gulled by a plausible fraudster. Despite the efforts of some to resurrect Kammerer’s reputation, notably the mystic and over-taken-notice-of Arthur Koestler with his book, The Case of the Midwife Toad, informed opinion seems to have swayed towards the view that Kammerer’s studies were fraudulent since there are plausible explanations as to how he, possibly with the assistance of others, had contrived to present doctored evidence that favoured his Lamarckian hypothesis.

There is a letter from George Albert Boulenger mentioned in Koestler’s book stating that Bles had visited Kammerer in Vienna at some time around 1908, so their meeting, at which all parties would have spoken German given Kammerer’s limited conversational English, would have been an opportunity to catch up. It would have been interesting to know if Hans Gadow (1855-1928) was also present. He helped Kammerer by translating the discussion at the Cambridge lecture but was not impressed by his science. Gadow was another amphibian enthusiast, notably writing the classic volume in the Cambridge Natural History series, but also keeping and breeding them at his house Cleramendi (since renamed) on Hinton Way at Great Shelford. I get the impression that Bles and Gadow were close; they operated as a team as two of the local organsers of the 1898 zoological congress held in Cambridge.

Both Kammerer and Bles had kept Olms, the cave-dwelling blind salamander of south-eastern Europe. Kammerer claimed to have bred them in captivity, a claim now strongly disputed since his ‘findings’ bear no relation to what has been observed either before or since, i.e. that they are viviparous and breed every year or so. Both had found that when kept in the light, the normally white animals turn black. Bles got there first on that one since Hans Gadow in his book published in 1901 wrote:

Mr. Bles has succeeded in producing several totally black specimens, having kept them for several months in a white basin under ordinary conditions of light. No experiments have yet been made to find out if the black pigment deposited is lost again in darkness.

Kammerer also claimed that eyes became larger when they were kept under alternating red light and daylight. When the skin over the eyes was removed, a specimen with normal eyes was produced. An alternative explanation, that he might have obtained such a specimen from a natural population in this highly variable species, has been advanced. However, Kammerer does not appear to have claimed that Olms with eyes or which had turned black produce young with these characteristics, as some neo-Lamarckists seem to have imagined.

Embed from Getty Images

In a previous post (here) I have described how it was intended to repeat and extend Kammerer’s experiments with Olms at London Zoo in the 1930s under the direction of Ernest W. MacBride, arch-lamarckist, Kammerer’s vicar on earth and a powerful, dogmatic but totally misguided figure in British science during the early decades of the 20th century. He also, incidentally, assumed the role of ‘Master of Ceremonies’ at the Cambridge lecture where it was said, ‘old MacBride’s ridiculous ex-cathedra statements did not help’.

Edward Bles was reported as having found Kammerer ‘absolutely honest’. However, he was clearly not convinced by what he had been told or had seen. After all he did insist that the chair he funded at Cambridge should be named after Darwin.

Bles did not live long enough to see the sad end of Kammerer; he died suddenly on 3 May 1926. Three months later, on 7 August, a letter to Nature by Gladwyn Kingsley Noble (1894 –1940) appeared. It delivered a bombshell: the alleged black nuptial pad of the only specimen of Kammerer’s Midwife Toad that was said to have survived was Indian Ink. Kammerer shot himself and was found dead on an Austrian mountain path on 23 September.

Alphen JJM van, Arntzen JW. 2016. Paul Kammerer and the inheritance of acquired characteristics. Contributions to Zoology 85, 457-470.

Gadow H. 1901. Amphibia and Reptiles. The Cambridge Natural History Volume VIII. London: Macmillan

Koestler A. 1971. The Case of the Midwife Toad. London: Hutchinson.

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 

Why is the human sex ratio 1:1 at birth?

Having found a dramatic shift in sex ratio at birth in one species of mammal, I have for decades kept an eye on discussions as to whether the human sex ratio at birth differs in some circumstances from 1 male: 1 female. Mammals in theory have two ways of controlling the sex ratio at birth: (i) at conception, or (ii) later by selectively reducing the number of young in utero. We found the latter mechanism at work in the guinea-pig. Since human litter size usually equals the  number of eggs and rarely exceeds 1 and since gestation is relatively long, it always appeared that if there were to be any maternal or paternal genetic control of the sex of the offspring it would have to be at the time of conception, rather than by selective death and reabsorption of embryo or fetus.

In the 1980s I once did the experiment of asking biologists from different disciplines why they thought the human sex ratio is 1:1. The reproductive biologists replied that it was just the result of random segregation of the sex chromosomes. The sex of a human offspring depends on whether it inherits and X or a Y chromosome from its father. Random segregation will, on average, result in a 1:1 ratio. By contrast, the evolutionary biologists said that the sex ratio is explained by Sir Ronald Fisher’s Principle: with the sex of a subject to genetic variation, the the sex ratio will always stabilise at 1:1. I will not repeat the simple explanation that can be found here.

Shifts of the of sex ratio at birth in various animals has been explained in terms of the Trivers-Willard hypothesis: parents which possess a heritable trait that benefits the lifetime reproductive success of one sex will bias the sex ratio towards that sex. There have been various claims in studies of human populations along these lines; for example, male-biased sex ratios in taller, wealthier, high status parents with the offspring likely to be more successful in competition for a mate. However, such claims have been controversial because of the statistical methods used and the results have often not borne out when larger samples were taken from the population.

Both the Fisher Principle and Trivers-Willard rely on there being genetic variation in the sex ratio, in other words that a bias towards one sex or the other is heritable. Thus a key test is to look for heritability in a very large human population. On standard scale of 0 to 1, ‘0’ denotes that a trait is not heritable while ‘1’ all differences in a trait can be explained entirely by genetic variation. Many traits fall somewhere between those two extremes.

But what does determine human sex ratio? It would be predicted if sex ratio is a heritable trait then Fisher’s Principle would apply. By contrast, if it is not heritable then simple Mendelian segregation of the sex chromosomes would suffice as an explanation.

Over the years there have been all sorts of suggestions and claims that the tendency in a family to produce offspring completely or partially biased to one sex is hereditary, and that particular genes could be involved. However, these conclusions have been criticised because the sample sizes were small and the statistical inferences drawn were invalid.

A recent, important paper has tackled the problem by using data from the entire population born in Sweden in and after 1932. That was 3,543,243 individuals and their 4,753,269 children. The results of the analysis were clear. There was no evidence of heritability at all. The calculated heritability was 0. In other words, there was no need to invoke Fisher’s Principle since with no heritability there can be no Fisher.

The authors summed up their results:

In sum, all of our results are consistent with the simple explanation that variation in offspring sex ratio in humans is due to unbiased Mendelian segregation of sex chromosomes during spermatogenesis and unbiased fertilization. The slight excess of male births is likely to be due to a general difference in survival of male and female embryos in the womb, the reasons for which are not yet understood.

Looks like my reproductive biology colleagues were right. Pity I can’t tell most of them; they are long dead.

The question now, of course, is whether the same conclusion, that the human sex ratio at conception is simply the outcome of random segregation of the sex chromosomes, applies to other or to all mammals? And are the statistically-robust demonstrated shifts in sex ratios at birth in some species and in certain environmental conditions all the result of differential loss of embryos and fetuses in utero? I shall permit myself to guess that the answers are ‘Yes’ and ‘Yes’ even though, as with previous human studies, there have been claims that the answer to the first question is ‘No’.

Zietsch BP, Walum H, Lichtenstein P, Verweij KJH, Kuja-Halkola R. 2020 No genetic contribution to variation in human offspring sex ratio: a total population study of 4.7 million births. Proceedings of the Royal Society B 287: 20192849. http://dx.doi.org/10.1098/rspb.2019.2849

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

The Journalist and the Giraffe. Chapman Pincher’s paper in Nature

There cannot be many journalists who still have a scientific paper they published in the 1940s quoted in current discussions on an old evolutionary problem. There is though one—Chapman Pincher†. He suggested a different interpretation to that then current on the evolution of the long neck of the giraffe, that exemplar used to enlighten schoolchildren on the difference between Lamarckian and Darwinian mechanisms of evolution.

I have previously covered Chapman Pincher’s early career as a biologist before he hit the big time as a science and defence correspondent for the Daily Express. It was only when I read further into his autobiography which he wrote shortly before his death in 2014 aged 100 (finding on the way the sources of his leaks of government information) that I learnt of his paper in Nature.

One of his sources for science stories was the joint-editor of Nature, Jack Brimble*. Brimble showed the content of each issue to Pincher before publication  and it was Brimble who in 1949 published his paper (then always as a ‘letter’ to Nature) on the origins of the long neck of the giraffe.

Jack Brimble

Pincher argued that a much better explanation for the long neck was not the selective advantage suggested by Darwin of being able to reach leaves in tall trees but because of the advantage of long legs in providing a longer stride and therefore a greater speed to escape predators. The neck had then to be concomitantly long in order for the head to be brought to ground level for drinking. Pincher wrote:

So, I suggested that, as with the evolution of so many animals, it was the predator-prey relationship which had been responsible, not occasional food dearths.

Frederic Wood Jones FRS (1879-1954) a classical anatomist, who had worked on all sorts of biological problems and phenomena from the formation of coral reefs to the lesions caused by judicial hanging, with very strange views on evolution and the value of genetics, wrote to the editor in reply to Pincher. Wood Jones pointed out that he and Robert Broom FRS (1866-1951)—the famous primate palaeontologist and anatomist also possessed of very strange views on evolution by ‘spiritual agencies’—had come up with the same idea as Pincher. The publications quoted were obscure: a book by Broom, Darwin and the Giraffe, published in South Africa in 1945, and an article by Wood Jones in the Manchester University Medical School Gazette of 1946. In post-war Britain it is not surprising that Pincher had not been aware of them.

Pincher’s paper is still discussed along with the original and more recent ideas on how the Giraffe acquired its long neck. A long paper argued it was the result of sexual selection while another disputed that claim. The giraffe continues to intrigue those seeking to determine the single or multiple selective advantages provided by an ever longer neck while at the same time providing false hope to the creationists whose beliefs infest the internet.

Me? Having watched Giraffes feeding in trees the wild numerous times, I’m still with Darwin for the initial selective advantage.

…and the take-home message for Chapman Pincher’s success:

his ‘Who knows wins’.

Reticulated Giraffe. Northern Kenya 1991

†Henry ('Harry') Chapman Pincher (1914-2014)

*Lionel John Farnham Brimble (1904-1965) 

Mitchell G, Sittert S van, Skinner JD. 2009. Sexual selection is not the origin of long necks in giraffes. Journal of Zoology 278, 281-286

Pincher C. 1949. Evolution of the giraffe. Nature 164, 29-30

Pincher C. 2014. Dangerous to Know. London: Biteback

Simmons RE, Scheepers L. 1996. Winning by a neck: sexual selection in the evolution of giraffe. American Naturalist 148, 771-78

Wood Jones F. 1949. Evolution of the giraffe. Nature 164, 323

Chinese Giant Salamanders: How many species are there?

Two well-publicised papers, published in 2018 and 2019, based on analysis of mitochondrial and nuclear genes, propagate the view that there is more than one species of giant salamander in China, that these species are ‘cryptic’ in that they do not differ in appearance, and that some are in imminent danger of extinction through ignorance of their existence. The authors certainly established that there are a number of distinct genetic lineages of giant salamander in China, enough to convince adherents to the phylogenetic species concept that they constitute different species. However, whether they are ‘good’ biological species is a matter that can be debated endlessly.

Giant salamanders in China in the wild are endangered because of over-collecting for the human food trade and from loss of habitat. Those working on the origins, evolution and conservation of these animals face major difficulties. The escape or release of wild-caught and farmed animals transported alive in large numbers throughout China in recent decades means that the geographical origin of newly-collected specimens cannot be guaranteed. By using specimens in museums collected before the vast increase in trade, the authors of the 2019 paper have overcome this problem but at a cost; the number of available specimens was small—just 17 individuals—since the DNA of many early specimens had been degraded by preservation in formalin.

The lineages are associated with the mountain ranges formed during the great geological upheavals that formed the Tibetan plateau starting about 3.3 million years ago. The authors of the 2019 paper realised that two of the lineages could be attributed to species that had been named in the past.

One lineage was be attributed to the classical domain of the Chinese giant salamander—in the northern Yangtze/Sichuan region—and conforms with Andrias davidianus. A second lineage from the Pearl River tributaries in the Nanling Mountains of south-eastern China appears to be that described by Edward George Boulenger in 1924 as a separate species, Andrias sligoi, that was later lumped into A. davidianus. A third lineage from the Huangshan mountains of north-eastern China has never been described as a separate form previously and could be a new, as yet un-named, species.

Boulenger noted morphological differences between what he named Megalobatrachus (now Andrias) sligoi and M. maximus. He would, wouldn’t he, since that is how new species were described then. But just as at the present with molecular genetic data, different people in the trade regarded some differences as too small to justify separation into a new species; others regarded the tiniest difference sufficient.

At that time Boulenger took his father's (George Albert Boulenger) view that any observable differences between Chinese and Japanese giant salamanders were too small to consider them as two species and continued to lump them into one, M. maximus. While he could find no consistent difference between the Chinese and Japanese forms, others claimed they could and the species maximus was split again into the Chinese, davidianus, and the Japanese, japonicus.

Ignoring the arrangement of tubercles on the head (which appear to differ somewhat in the Chinese and Japanese species) Boulenger also differentiated sligoi by its longer, flatter, and smoother head, and by the shorter distance between the eye and lip.

How Boulenger distinguished his new species, M. sligoi

Boulenger’s new species did not survive as such. Later authors argued it was no different or insufficiently different from davidianus and into the latter it was lumped. Liu in his Amphibians of Western China, published in 1950, condemned Boulenger’s erection of sligoi as a separate species:

Neither the length of the head (which is difficult to define, and which was not defined by Boulenger) nor the relative distance of the eye from the labial border are valid characters.

But Liu did not say why the characters are not valid!

We therefore seem to have agreement between morphology (whether declared ‘valid characters’ or not) and molecular genetics published 95 years later. However, I too have doubts about Boulenger's comparison (see later article). But Boulenger may have been right all along, and the name given recently, South China Giant Salamander, Andrias sligoi, an appropriate one. However, that is only if you agree that species should be defined in that way and not by the biological species concept.

Before accepting the increased number of proposed giant salamander species, perhaps it is worth considering whether the results of the recent artificial mixing up of lineages in both China and Japan (A. davidianus has been released into Japan) have not already invalidated that proposal.

‘Good’ biological species do not or only rarely interbreed in the wild. The classic difficulty with deciding whether species whose ranges do not overlap (i.e. they are allopatric) are ‘good; biological species, is that they do not meet in the wild, and the question of if, say, a geographical barrier were to be removed, would they interbreed naturally, cannot be answered. However, if lineages interbreed freely after translocation, then the case for their being biological species is severely dented if not holed beneath the waterline. Indeed, in the 2018 paper, the authors, do show that hybridisation between lineages has occurred in farms. Similarly, hybridisation between Chinese and Japanese forms has occurred in Japan where the former has been introduced.

On the evidence of hybridisation, then, the case for a number of ‘good’ species of giant salamander, according to the biological species concept, is weak.

The authors of the two papers (many of the authors are common to both) are concerned, rightly, with the conservation of giant salamanders and with the measures that should be taken to ensure their survival in the wild. However, the type of evidence used—that different lineages equal different species—is clearly not acceptable to adherents of the biological species concept. Indeed, if it that premise were correct, two of my daughters-in-law would be of a different species to me and my grandchildren interspecific hybrids. Thus, Jerry Coyne, a world authority on speciation from the University of Chicago, in his blog, Why Evolution is True, wrote:

…virtually every paper I’ve seen on the process of speciation—that is, on the ways that new species come into being—deals not with the accumulation of genetic distance per se, but on the development of reproductive barriers that eventually prevent populations from exchanging genes.

Greg Mayer of the University of Wisconsin, making the same general point from a different case on Coyne’s website:

…At the time, this bothered me, as I saw it as an application of the old morphological species concept, extended to genetic data: if you can tell them apart, they are different species. This is also what Jerry argued against… an arbitrary amount of morphological or genetic difference, or inferred time of separation based on the amount of genetic difference, is not a sound basis for a species concept.

Here, sadly, there may be incompatibility between the politics of conservation and science. Conservationists find it easier to provoke politicians into action with measures to protect species rather than populations and habitats—thus the more species, the better the argument and the greater geographical spread of habitat protection.  However, Jerry Coyne has argued cogently:

…the ‘splitting’ of species [in this case discussing the Giraffe, ‘split’ into different ‘species’ by virtue of differences in genetic lineage] is a conservationist motivation, not an attempt to partition out nature in biologically and evolutionary meaningful ways’.

The research on the giant salamanders reminds us of some fundamental biological questions, like the perpetual problem of how we define a species, as well as some urgent practical conservation concerns. Indeed the research highlights the urgent need to protect, manage and re-introduce populations of giant salamanders in the wild.

However we regard Boulenger’s Megalobatrachus (now Andrias) sligoi, the discovery of his type specimen is an interesting story that I will cover in a further article…and can we determine where those giant salamanders used for class dissection in Hong Kong in the 1960s came from?

Boulenger EG.. 1924. On a new giant salamander, living in the Society’s gardens. Proceedings of the Zoological Society of London, 1924, 173–174 

Turvey ST, Marr MM, Barnes I, Brace S, Tapley B, Murphy RW, Zhao E, Cunnigham AA. 2019. Historical museum collections clarify the evolutionary history of cryptic species radiation in the world’s largest amphibians. Ecology and Evolution 2019;00:1–15. https://doi.org/10.1002/ece3.5257

Yan F, Lü,J, Zhang B, Yuan Z, Zhao H, Huang S, Wei G, Mi X, Zou D, Xu W, Chen S, Wang J, Xie F, Wu M, Xiao H, Liang Z, Jin J, Wu S, Xue C, Tapley B, Turvey ST, Papenfuss TJ, Cunningham AA, Murphy RW, Zhang Y, Che J. 2018. The Chinese giant salamander exemplifies the hidden extinction of cryptic species. Current Biology, 28, R590–R592. https://doi. org/10.1016/j.cub.2018.04.004 

How Birds Survive at Sea. The (incorrect) view from the 1930s in a popular article from a renowned ecologist

Occasionally I see a paper or article that I wish had had seen earlier. This is one of them.

Animal and Zoo Magazine, under its earliest title, Zoo, had the great advantage Julian Huxley as its advisory editor and backer with the Zoological Society of London. He could get former colleagues and students from Oxford—very often the leading zoologists of the 1930s—to write articles describing for the general public their research in a wider context.

The sixth issue of the magazine in November 1936 contained an article on seabirds. It is one I wish I had seen in the 1960s or early 70s since I would have quoted it in our book on salt glands for the then current view of how seabirds survive at sea, before, that is, Knut Schmidt-Nielsen discovered salt glands in the 1950s and really explained how they did it.

The title was ‘Wings Over the Sea’ and the author was Vero Copner Wynne-Edwards (1906-1997). He was then at McGill University in Canada, formerly at Oxford, the marine laboratory in Plymouth and Bristol University. He described very well what was then known of the natural history of seabirds. He included some of his own research on their distribution nearer or farther from land, which contributed to his election to the Royal Society in 1970, and stressed the differences between, say, gulls, which never move far from a source of freshwater to others from far out in the oceans which appeared to survive without freshwater. He explained the prevailing view: ‘As a group, birds are no more able to drink salt-water than mammals, and a diet of salt water instead of fresh is quickly fatal to those land birds with which experiment has been made’ and ‘In the ordinary combustion of food substances, the principal end-products are carbon dioxide and water; and it is possible that by exercising the most rigorous control of water excretion, other birds and mammals which live permanently out of reach of fresh water manage to make do with what they derive from this internal source. They may also, however, be able to manufacture fresh from salt water in their kidneys and cloaca’.

Later, after salt glands had been discovered, a general relationship emerged between the size of the salt glands and Wynne-Edwards’s ecological classification of seabirds and their habitat. Thus those that occur inshore have smaller salt glands than those that range to the edge of the continental shelf which in turn have smaller glands than the truly pelagic species, like albatrosses. What is important to remember is that all seabirds have salt glands that can be activated within minutes of having to ingest sea or estuarine water or invertebrate prey high in salt. Ecological questions though do remain. For example, removing excess salt via the salt glands is energetically expensive, and so what is the trade-off in inshore birds between flying back to land and a source of fresh water (which Wynne-Edwards described in gulls) or staying out at sea and letting the salt glands operate?

V.C. Wynne-Edwards
(from Newton - see below)

Wynne-Edwards who, in this popular article, was quoting the views of physiologists of the time was a renowned practitioner of the observational natural history approach to ecology rather than the experimental or quantitative. Nearly 25 years after writing this article he was Professor of Zoology at Aberdeen. There he wrote his book, Animal Dispersion in Relation to Social Behaviour, which was published in 1962, a book that contained a revolutionary idea in evolutionary biology that was to be shot down in flames and to remain shot down. Wynne-Edwards proposed the idea of ‘group selection’ from his work on birds—that animal populations collectively regulate their own numbers in order to prevent the overexploitation of their resources. The gatherings of birds from whole areas in communal gatherings he interpreted as means of assessing the size of the population by its members. A group breeding to excess and therefore profligate with its resources would be selected against while one that regulated its numbers would have, in the long-term, greater success.

The idea of natural selection operating on a group, rather than on an individual, was, of course, contrary to accepted Darwinian views and it was not long before the killer flaw in Wynne-Edwards’s hypothesis was spotted: a group of animals behaving in the restrained, conforming way that he proposed would be unable to resist invasion by a selfish genotype, i.e. one that did not conform. In short, the selfish would outbreed the selfless social conformer.

Despite being shot down, the book was very influential and more biologists than would later admit to were rather attracted to its tenets since the cosy social organisation it implied often matched the political world view of the readers as to how human beings should behave.

Wynne-Edwards stuck to his ideas throughout his life, in print that is. He was reluctant to discuss his views with others, even refusing to take questions at the end of an invited lecture or seminar. Sadly, his obituarists concluded, group selection had become an article of faith.

In the 1980s I met Wynne-Edwards in Aberdeen a couple of times. I was also struck by his aloof demeanour and unwillingness to engage on any topic, even after a glass or two. My impression was that he actually had rather a hard time as head of a university department and Regius Professor—and he was known to stand on ceremony—whose big idea had been so publicly and so effectively pooh-poohed. So I actually felt rather sorry for him. It seemed to me, from reading the hoo-ha over his book in the 1960s and later, that he had taken the interpretation of his observations too far and that instead of publishing his hypothesis in a fully-formed book he should have first explored his developing ideas more openly at conferences and with others interested in the overall problem.

But then, finally, I got another impression of Wynne-Edwards. My late assistant was visiting her mother-in-law in a care home in Banchory. There she had tea with her mother-in-law’s new-found friends—the Wynne-Edwards. She told me of this the next day and of how welcoming and friendly they were. In later visits (I had told her the history of group selection) he explained something of his earlier work on seabird distribution and on fisheries, the human management of which, of course, parallels his ideas on the natural control of populations.

Wynne-Edwards VC. 1936. Wings over the sea. Zoo [Magazine] 1 (6, November 1936), 18-21.

Paul Racey’s obituary for the Royal Society of Edinburgh can be found here.

Newton I. 1998. Vero Copner Wynne-Edwards, C.B.E. 4 July 1906–5 January 1997. Biographical Memoirs of Fellows of the Royal Society 44, 473-484.

Sea snakes and burrowing eels

Sea snakes are fascinating animals. There were a number of dead ones pickled in jars in the old Northcote Science Building of the University of Hong Kong. They had been gathered from the nets of the fishing fleet or the fishery research vessels. It was difficult to make out the form and original coloration of the pickled specimens. The most interesting, of which there were photographs, was one with a tiny head, thin neck but wider body. I now realise it was the Slender Sea Snake, Hydrophis, now Microcephalophis, gracilis, and could well have been the same preserved specimen used as an illustration in Hong Kong Amphibians and Reptiles. The timing is right since it was the only specimen caught in Hong Kong waters—in 1963 in Deep Bay.

The preserved specimen of the Slender Sea Snake used in
Hong Kong Reptiles and Amphibians. I have added the
red ellipse to show the very small head and thin neck

But why the small head and thin neck in many species of sea snake? The old idea, which turned out to be a ‘just-so’ story, was included on the short section on sea snakes (there was not a single photograph) in Schmidt & Inger’s 1957 book, Living Reptiles of the World:

It is remarkable that some of the longest of the sea snakes have a small head and slender neck and anterior half of the body, with a bulky abdominal portion that is very much larger in diameter. This curious body form, which recalls that of the extinct marine plesiosaurs, seems to be associated with the mechanical requirements for striking at prey in the water. Without any fixed fulcrum from which to launch its stroke, the free-swimming venomous snake makes use of the inertia of the heavy abdomen, while the great resistance of the water is made less by the slenderness of the head and neck…

Later, Harold and Helen Voris of the Field Museum in Chicago examined data on what species of fish the various sea snakes prey. They found that a large number of species eat eels. Subsequently it was found that the snakes with a small head feed on burrowing eels and gobies, and those with a very small head feed virtually exclusively on burrowing eels. Divers have also reported seeing some species of sea snake with their heads in a burrow. Therefore, it has become clear that the small-head-thin-neck type of sea snake is adapted to entering the long burrows of eels and emerging with a meal.

Along with their various physiological adaptations to life at sea, which I will not go into further here,  and the specialized feeding habits—including species which feed exclusively on fish eggs—a significant feature of sea snakes is the number of species within a relatively small geographical area. A recent paper* relates feeding on burrowing eels to the rapid increase in the number of species. The pursuit of a previously untapped food source has been well established in other animals as a trait that would be favourably selected and, therefore, act as a driver of speciation.

From*. I have added a red ellipse to highlight the differences in the width of the head and neck

There are more than 60 species of sea snake. A rapid speciation, accounting for 60% of known species—the fastest known amongst reptiles—occurred from about 7.5 million years ago. The change in body form associated with feeding on burrowing eels appears to have occurred in six or seven of the lineages determined by genomic analysis. In other words, there is strong evidence of convergent evolution.

The authors conclude:

Our study has revealed that trophic specialization has had a strong influence on body morphology in sea snakes, and this relationship is predominantly driven by the convergent evolution of microcephalic burrowing eel specialists. Dietary specialization appears to invoke strong selective pressures that manifest as predictable and rapid morphological changes. Future studies are needed to examine the genetic and developmental mechanisms underlying these dramatic body shape changes and address their role in speciation. 

Then I started to think about implications for how the small-headed sea snakes feed. Let’s assume the diameter of the neck equals the diameter of the eel’s burrow. If the snake swallows the eel (the diameter of the burrow) while in the burrow its neck will be twice the diameter of the burrow and it could get stuck. Therefore, is it perhaps more likely that the snake pulls the eel out of the burrow before swallowing it? But, if alive, the eel would stand a chance of escaping, so is that why the venom of these sea snakes is so powerful? To ensure that the eel is dead before being pulled from its burrow and to enable a quick kill by a snake that must swim to the surface in order to breathe? Alternatively, perhaps the snake only enters burrows that are wider than its neck. Then it could, perhaps ingest its prey without getting stuck. But a large eel in a large hole might then be too big to be swallowed by the small head (the maximum width of prey has been found to 1.5 times that of the neck)? Divers or remote cameras watching how these small-headed sea snakes feed may be the only ways of providing an answer.

The dangers of a snake swallowing its prey with its neck in a confined space was brought home to us on Boxing Day 1966 in Hong Kong. We were walking along Conduit Path a short distance from the top of University Drive when we found a dead rat snake with its head in a small hole in the bank. A good pull was needed to extract the snake. It was in process of swallowing a toad and the swollen throat had jammed the snake plus toad in the entrance to the hole. We could only assume that the oxygen within the small hole had run out and the snake had asphyxiated itself as it tried to retreat. Unwisely, with hindsight, we left the snake plus toad on the bank of earth, intending to pick it up on the way back from our walk and preserve it in the lab. But it had gone; some scavenger had made off with it.

*Sherratt E, Rasmussen AR, Sanders KL. 2018. Trophic specialization drives morphological evolution in sea snakes. Royal Society Open Science 5, 172141. http://dx.doi.org/10.1098/rsos.172141 

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

Peaker M, Peaker SJ. 1968. Death of a snake while swallowing prey. British Journal of Herpetology 4, 38-39. 

Schmidt KP, Inger RF. 1957. Living Reptiles of the World. London: Hamish Hamilton.

Voris HK, Voris HH. 1983. Feeding strategies in marine snakes: an analysis of evolutionary, morphological, behavioral and ecological relationships. American Zoologist 23, 411-425.