Salt glands and Sea Water: Duck Farming in 1960s Hong Kong and a Giant Petrel in Argentina

Salt-glands enable many birds to drink saline waters and eat salt-rich invertebrate foods. A question that arises is the extent to which the salt gland is used in birds that can fly or swim to a source of fresh water to drink. Do they just stay in salt water and get rid of the salt through the salt glands, or do they, if possible, go to fresh water to drink? Salt glands—just like man-made desalination plants—need a great deal of energy to run, so one might predict that birds with salt glands would, if they could, drink fresh water. There could be a trade-off, of course, between using energy to fly or swim to fresh water and using energy to stay put with the salt glands working.

Several weeks ago I wrote about an article by V.C. Wynne-Edwards in a magazine of the 1930s—before the discovery of salt glands in the 1950s. He had found that gulls do not, in general, stray too far from a source of fresh water and suggested that they only drink there.

The first actual observation I heard of was in Hong Kong in the 1960s. Domestic ducks and geese have salt glands and given salty water to drink can switch them on in a matter of minutes. They cannot, however, unlike truly marine birds, survive on full-strength sea water for any length of time.The late John Phillips (1933-87) was appointed Professor of Zoology at the University of Kong Kong in 1962 at the age of 29 . He had previously worked on salt glands for a while and soon after his arrival in Hong Kong had been driving through the New Territories when he saw a large flock of domestic ducks dabbling for food on salt flats near Yuen Long. He thought the salt glands must have been well and truly working in those birds. That may indeed have been the case, temporarily at least, since although mechanical arrangements in the beak can reduce the ingestion of water along with food, the ducks must have been taking in some water nearly as salty as sea water. However, as he continued watching the farmer appeared and herded the ducks back to his land. The ducks ran onto the farm and headed straight for a container of fresh water which they drank avidly.

I had been planning to write this article but lacked a photograph of a flock of domestic ducks in Hong Kong. Then Rob Taylor posted this photograph in a Facebook Group on Hong Kong in the 1960s; I show it here with his approval. The ducks appear to be sitting on the bank of a gei wai—an artificial salt water pond filled by the waters of the Pearl River estuary and used for rearing salt-water shrimps.

Domestic ducks- New Territories, Hong Kong.
Photograph from Rob Taylor's family collection

I saw something similar in in a very different setting with a very different species. New to the birds of the southern ocean, I was keeping my eye on a Southern Giant Petrel (Macronectes giganteus) as we walked along the shore in Ushuaia in southern Argentina. The wind was icy and as I pulled a scarf around my mouth—I had raging toothache—I noticed the petrel moving close inshore. It made for a drain from which fresh water after a heavy shower was flowing into the sea. The bird had a long drink from the drain and headed paddled off to sea. 

Thus in both the domestic ducks and the petrel, fresh water would have diluted any excess salt in the body and enabled excretion of dilute urine through the kidneys rather than concentrated salt from the salt glands.

These observations on birds drinking fresh water in preference to salt water accord with experiments that have been done. Most birds tested—even a number that have salt glands—prefer fresh water to salt water when offered a choice. A possible exception is an albatross that is truly oceanic.

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.

Salt Glands in Iguanas; Video footage of a South American iguana swimming along a reef

The metaphorical ink had hardly dried on my post (22 March 2019) about salt glands in Galapagos Marine and Land Iguanas and their hybrids when my attention was drawn to a recent video of a common South and Central American iguana, the Green or Linnean Iguana (I. iguana), swimming along a reef off Curaçao.

It's not everyday you spot a land iguana roaming the reef in Curaçao 🦎. 🎥 : IG user turtleandray_photography pic.twitter.com/RzoNE5fZJ3

— PADI (@PADI) 1 April 2019

The question raised, of course, is: was it was feeding on the reef. I am sure that iguanas could swim for hours in sea water without taking in any sodium chloride but eating is a different matter since, like the Galapagos Marine Iguana it is difficult to see how ingestion of sea water could be avoided.

Fundamental questions about the salt gland of a number of iguanid lizards, which appear to be able to swap between a high sodium to a high potassium secretion according to diet or salinity of water ingested, remain unanswered. Some of the questions may be basic, for example, do high sodium and high potassium secretions come from the same gland in the head, or the same cells of one gland? We need some proper physiology and cell biology to find out. And more observations from divers of the type shown in the video.

For more information on the sighting of iguanas in the sea, see Greg Mayer’s post on Jerry Coyne’s WEIT here.

Galapagos Iguana Hybrids: What about their Salt Glands?

Last week I gave a talk on salt glands to a local group. I remembered that I had not raised a question here that arises from the existence of some very odd animals on one island of the Galapagos.

Everybody knows there are the Marine Iguanas (Amblyrhynchus cristatus) and Land Iguanas (Conolophus sp.) on the Galapagos Islands. Evidence indicates they had a common ancestor about 4.5 million years ago. Watchers of television wildlife programmes cannot fail to have noticed the entirely different lifestyles. Land iguana eat plants and do not venture into the sea. By contrast, Marine Iguanas eat seaweed often foraged at considerable depths.

Over the past forty years it became evident that on one very small island, Plaza Sur, just off the east coast of Santa Cruz (Indefatigable) there were hybrids present between Marine and Land Iguanas (Conolophus subcristatus). These hybrids are sterile as one might expect. There is good evidence that their fathers are male Marine Iguanas, their mothers Land Iguanas. It seems that the breeding seasons of the two species can overlap there. The habitats are very not very far apart either, the thin vegetation where the Land Iguanas bask and feed being only a matter of yards from the rocks on which the Marines bask.

We took video and still photographs of one of these hybrids on Plaza Sur in January 1012. It was lying with Land Iguanas. Local guides say they are not very active and typically have a ‘spaced out’ look like the one below:

Hybrid Marine x Land Iguana, Plaza Sur, 12 January 2012

For comparison: Galapagos Land Iguana, Plaza Sur, 12 January 2012

Also for comparison: Galapagos Marine Iguana, Plaza Sur, 12 January 2012

Nesting burrows of Land Iguanas. Plaza Sur, 12 January 2012

Vegetation on Plaza Sur, 12 January 2012. The marine iguana-like claws of the hybrid iguanas are said to be advantageous in reaching the fruits of the prickly pear. The land iguanas have to wait for them to drop

The question I have had since then is what do the salt glands of these hybrids do? Marine Iguanas have very active salt glands which operate to remove the sodium chloride ingested during feeding. In addition, the concentration of potassium is about ten times higher than in birds which could reflect the high potassium concentration in the plants of their diet. Marine iguanas on land can be seen snorting secretion from the salt glands out of their nostrils, a phenomenon observed by Charles Darwin who did not appreciate its significance to their survival.

Other, species of iguanid lizard have salt glands that can secrete both sodium and potassium. There is evidence that the ratio can be changed by varying the diet. Lizards on a high sodium diet or given a salt load produced a secretion with a more sodium than potassium. As far as I am aware, the Land Iguanas of the Galapagos have not been studied in this respect.

The hybrids seem to live and eat like their Land mothers although I see there are anecdotal reports of their being seen eating seaweed but not entering the water to do so.

So do the hybrid iguanas on Plaza Sur have functional salt glands? How does their size compare with the Marine and the Land? If the salt gland is functional, what are the stimuli for secretion, and does the ratio of sodium:potassium change to reflect changes in the dietary intake?

Possibilities of studying the hybrids to answer these questions are low but the insights into which genes are involved in salt-gland structure and function would be fascinating outcome of this ‘natural experiment’ but biological dead end.

I  used this drawing from Bill Dunson's paper in our book on salt glands

Mabel Hokin and Salt Glands: My sad demolition of a biochemical treasure

Having worked on bird salt glands in Hong Kong I arrived at Babraham in October 1968 to work on the mammary gland and the mechanism of milk secretion—a very different gland and a very different fluid being produced.

During that summer Jim Linzell had attended a satellite symposium of the Washington Physiological Congress on exocrine glands and had heard Mabel Hokin give a talk on the bird salt gland. He told me about this and since a similar approach might provide information on the mechanism of secretion of the aqueous phase of milk, I set about doing similar studies on the mammary gland. However, when I read Mabel Hokin’s work in greater detail I realised there were some anomalies. I will not go into great detail but the concentrations of sodium, potassium and chloride ions in salt-gland slices appeared to be much higher than those reported by others. This mattered since by calculating the concentrations inside the cells from a knowledge of the size and composition of the extracellular space, she concluded that the high concentration difference of sodium chloride was established between blood and the inside of the cell, not between the cell and the lumen of the gland, as previous evidence had suggested. I, egged on by Jim Linzell and Richard Keynes FRS who was then Director of the institute and gathering information for his masterly review of ion transport mechanisms across membranes in different organs, thought it wise to repeat the Hokin experiments.

I was unable to get the same results as Mabel Hokin. The concentrations inside the cell appeared similar to other non-nervous tissues, implying that the high concentration gradient for salt is set up between the cell and the lumen of the gland, the later leading to the duct system and the flow of salt-rich fluid to the outside world.

The difference between mine and her results rested on the crude concentrations of sodium, potassium and chloride in the tissue, before any calculation of concentrations inside the cells. I did all sorts of studies with other tissues to see if the methods I was using gave results different from those reported by others. They didn’t. Were the salts being liberated from the tissue fully before analysis? Yes. I did all the standard tricks of analytical chemistry to check that when I added a known amount to the samples I recovered that same amount during analysis. Was I making a stupid arithmetical error in calculating the concentrations? I persuaded three colleagues to work through the calculations independently; they got the same answers.

I was—and still am—at a lost to explain how Hokin found such high concentrations of all three ions of interest. However, it is interesting that her concentrations in tissue were on average 1.94 times higher; double, in other words. Richard Keynes and I concluded privately that somewhere along the line Mabel Hokin had got her sums wrong by a factor of 2. In the days before spreadsheets and even before electronic calculators came into use, the chances of systemic error were increased. Keynes himself hogged the first computer (Olivetti Programma 101) to be installed at Babraham to recalculate some figures on ion movements across an epithelium or membrane originally worked on by a co-worker. ‘Well’, he said after his marathon session, ‘they were out by a factor of 10—100 in one direction and 1000 in the other’.

After the publication of my results, I sent Mabel Hokin an offprint but I received no reply. Her ideas on how the salt gland might work were not heard of again. But why was she working on the salt gland at all?

Mabel Hokin had a very interesting personal history as well as a key role in the uncovering of a major biochemical mechanism by which signals are passed within cells, even though she did not realise it at the time.

Sir Hans (then Professor) Krebs had an enviable reputation when he was at the University of Sheffield (before his defection to Oxford) of employing school leavers as technicians and then seeing the good ones through a university degree course and postgraduate research for a PhD. A number stayed with him as fully-fledged scientists for decades, or nested successfully elsewhere. Mabel Hokin was one of those school leavers.

Mabel Hokin the 1980s
Photograph used on Wikipedia

According to a potted biography on Wikipedia. Mabel Neaverson was born in Sheffield in 1924 to working-lass parents. Throughout her life she suffered from an autoimmune disease. After spending 1942-43 in the Land Army she joined the Krebs Cell Metabolism Unit as a technician in 1943. In 1946 she became an undergraduate student (funded at least in part by Sheffield Education Committee) and in the same year married her first husband, the actor, playwright, critic and university lecturer Dennis Davison* (1923-1994); he was also at the University and they met through her interest in costume design and the theatre. Her political activities at this time in the socialist society at university (Chairman, 1947-48) and as a member, with Davison, of the Communist Party of Great Britain were to have consequences a few years later. 

After graduation in 1949 (II(i) Hons. Physiology) Krebs suggested she should continue as a research student. Her supervisor was Quentin Gibson (1918-2011, FRS 1969) then in Physiology—apparently unhappily—at Sheffield. Her PhD, funded by the Medical Research Council) was awarded in 1952. I have only found one publication from that period which shows she was working on acetate metabolism in pigeon breast muscle.

As she started her PhD, Lowell Edward Hokin (1924-2018^†) was arriving in Sheffield from the U.S.A., accompanied by his first wife, to work with Krebs. Then, as the Wikipedia entry reads: ‘In a short time, Mabel met Krebs' graduate student Lowell Hokin, and the two began a romantic as well as professional relationship’. Divorces were obtained; they were married in Canada in December 1952 where they had arrived from Sheffield in April.

Rather than McGill University in Montreal, they had hoped to move from Sheffield to the U.S.A. but Mabel’s entry was completely blocked during the McCarthy era because of her communist party membership. 

In experiments started at Sheffield and completed in Montreal they found that when pancreatic slices were induced to secrete digestive enzymes by cholinergic neurotransmitters, radioactive phosphorus was incorporated at a greater rate into a chemical fraction of the cell they thought was RNA. However, the radioactive label was not in RNA but in the phospholipids of the cell membranes. Until then the phospholipids were ‘regarded as inert structural components of membranes’. Later, they showed the particular phospholipids that were labelled. The Hokins were the first people to demonstrate lipid turnover caused by the stimulation of receptors on the cell. The phenomenon became known as the ‘PI effect’.

The significance of the phenomenon they had discovered was not uncovered for some years. And this is where their own work took a turn in completely in the wrong direction. Because the PI effect was apparent in other organs when stimulated to secrete, they thought that the phospholipids must be involved in transporting substances across cell membranes. Because it occurred in organs like the newly-discovered salt gland which do not secrete enzymes they argued that their phenomenon must constitute the pump which needs energy to carry sodium across cell membranes. They erected a scheme called the ‘phosphatidic acid cycle’ which, they argued, carried sodium from one side of a membrane to the other. Their hypothesis received a great deal of publicity at the time with papers in Nature and Scientific American. But then their whole scheme fell apart. All sorts of evidence accumulated to show that their phosphatidic acid cycle did not fit the bill as a transporter of ions. The world moved on. But that is how Mabel Hokin came to work on salt glands. The announcement of the discovery of salt glands by Knut Schmidt-Nielsen in 1957 coincided with the Hokins seeking an organ that secreted sodium at a high rate and that was stimulated by cholinergic nerves.

Eventually, the ban on Mabel’s admission to the U.S.A. was lifted and the Hokins had moved from Montreal to the University of Wisconsin at Madison in 1957. This is not the place to describe their later work other than to point out that they were divorced in 1971, shortly after the work on the phosphatidic acid cycle as a transport mechanism was ended and the notion shot down.

The ‘PI effect’, however, took off, as described by Bob Michell FRS in his obituary of Mabel written for Biochemist shortly after her death in 2003:

Mabel and her scientific partner and ex-husband Lowell Hokin were amongst the few scientists who have initiated a new scientific field. Their work on stimulated phosphoinositide turnover in secretory tissues, most crucially in the 1950s and 1960s, was a slow fuse that finally ignited an explosion of work that made inositol phospholipids into star players in transmembrane signalling and many other cell regulatory processes. The extraordinary versatility of phosphoinositides would have come to light at some time without their work, but it is not clear how, and it would have taken much longer… 

It took another decade for the research community to realize that the initiating event of the Hokins’ ‘PI response’ is phospholipase C-catalysed hydrolysis of PtdIns(4,5)P2, which many cell- surface receptors harness as their central signal-transducing event. Later, 3-kinase-catalysed formation of PtdIns(3,4,5)P3 emerged as a second widespread signalling reaction, and a plethora of other roles for phosphorylated derivatives of PtdIns in central cell functions have since been uncovered. 

Mabel and Lowell Hokin laid the foundations on which all of these recent discoveries stand…She and Lowell never deduced exactly what their observations meant, largely because they were doing experiments that were ‘ahead of their time’, but those of us who followed could confidently use their beautiful results to develop new interpretations. 

Mabel was a gregarious and enthusiastic woman who never lost her North Country bluntness. Even when on crutches after having new hip joints, she would be dancing at a meeting party soon after coming off a long flight…

After I first read that I felt like I had shot Bambi.

The only photograph I have found of Mabel and Lowell Hokin at about the time they were working on
salt glands. A meeting in March 1966 on the Neural Properties of Biogenuc Amines

*Davison went to Australia in 1957 eventually becoming Senior Lecturer in English at Monash University in Australia.

†Lowell Hokin died last month (6 September 2018) in Colorado.

Hokin MR. 1967. The Na+, K+ and Cl content of goose salt gland slices and the effects of acetylcholine and ouabain. Journal of General Physiology 50, 2197-2209.

Hokin MR. 1969. Electrolyte transport in the avian salt gland. In, Exocrine Glands. Proceedings of a Satellite Symposium of the XXIV International Congress of Physiological Sciences. Edited by Botelho SY, Brooks FP, Shelley WB, p 73-83. Philadelphia: University of Philadelphia Press.

Keynes RD. 1969. From frog skin to sheep rumen: a survey of transport of salts and water across multicellular structures. Quarterly Reviews of Biophysics 2, 177-281.

Kresge N, Simoni RD, Hill RL. 2005. A role for phosphoinositides in signaling: the work of Mabel R. Hokin and Lowell E. Hokin. Journal of Biological Chemistry 280, e27.

Michell R. 2003. Mabel R. Hokin (1924–2003). Biochemist, December 2003, 62-63.

Peaker M. 1971. Intracellular concentrations of sodium, potassium and chloride in the salt-gland of the domestic goose and their relation to the secretory mechanism. Journal of Physiology 213, 399-410.