1957-2017: The Diamond Jubilee of Salt Glands: Knut Schmidt-Nielsen’s co-authors

In the last post I covered the history of the discovery of salt glands in birds by Knut Schmidt-Nielsen.  But who were his collaborators in the first salt-gland research, Carl Barker Jörgensen and Humio Osaki at the start, and then Ragnar Fänge?

Carl Christian Barker Jörgensen (1915-2007) was well known internationally as an animal physiologist but the only biography I have been able to find is in Danish. Therefore, Google Translate has had to come to my aid.. In 1940 he received Copenhagen University’s gold medal in zoology. He then assisted Holger Valdemar Brøndsted (who later had a chair in zoology at Copenhagen) at a school in Birkerød from 1941 until 1945 when the war ended. Jörgensen returned to Copenhagen and became assistant to Hans Ussing, of the eponymous Ussing Chamber, who was entering his heyday as the master of transcellular ion and water transport through his work on frog skin. Jörgensen himself looked at the effects of posterior pituitary hormones on salt and water movements.

Jörgensen remained at Copenhagen where he was professor from 1965 until he retired in 1985, pursuing a number of interests from suspension feeding, through salt and water metabolism to reproductive endocrinology. Most of his research was on the Common Toad, Bufo bufo. During the 1990s he published three major reviews including one on on the function of the bladder—huge in tortoises—from a historical perspective.

Humio Osaki (1916-2005) was in later life a medical protozoologist. In 1957 he was a research associate at Duke University working with Bodil and Knut Schmidt-Nielsen. How he came to be there I do not know because he had qualified in medicine in 1942, served as a medical officer in the Imperial Japanese Army until 1946 and then as a hospital clinician. After Duke University he was in academic medicine in Japan, finally at Tokushima and Kochi medical schools. As well as the paper on salt glands, Osaki also published with Bodil Schmidt-Nielsen on urea excretion in sheep, one of the key steps in the discovery of urea secretion (as opposed to simple filtration) by the mammalian kidney. Another co-author on Bodil’s urea paper is Roberta O’Dell who can be seen in a photograph helping in the salt-gland work with Osaki and Knut.

Humio Osaki (centre) with Roberta O'Dell and Knut
Schmidt-Nielsen working on salt glands in a gull at
Mount Desert Island(from Evans DH. 2015. Marine
Physiology Down East: The Story of Mt Desert Island
Biological Laboratory. New York: Springer

Humio Osaki working with Bodil
Schmidt-Nielsen on urea excretion (from here)

In the second phase of the salt-gland work, Ragnar Fänge (1920-1999) looms large. Another well-known animal physiologist who worked mainly on fish, he was another Scandinavian, this time Swedish. However, I have been able to find very little about him. I met him a few times but discovered nothing of his background or how he came to be involved with Knut Schmidt-Nielsen and salt glands—and I also forgot to ask Knut the same question. He was professor of zoophysiology at the University of Gothenburg in Sweden from 1962 until 1985.

And so a Norwegian (KS-N), a Dane (CBJ), a Swede (RF) and a Japanese (HO) made history.

1957-2017: The Diamond Jubilee of Salt Glands: Knut Schmidt-Nielsen's Major Discovery

As i wrote in this post on Bill Sladen, this year, 2017, marks the 60th anniversary of the announcement of the discovery of salt glands by Knut Schmidt-Nielsen and the publication of an abstract describing the work in Federation Proceedings. The talk was given to the American Physiological Society at the Federation of American Societies for Experimental Biology meeting in Spring 1957. A search shows this meeting was held in Chicago on 15-19 April. I also found from the bibliography published alongside his obituary as a Foreign Member of the Royal Society that he had also given a paper in 1957 to the Elisha Mitchell Scientific Society in North Carolina and an abstract was published* (which I have not seen); he was by then based at Duke University in North Carolina.

Salt glands are still fascinating: they turn on within minutes of excess salt being detected in the blood; although small in size they can secrete concentrated salt solutions at a very high rate, and to support this blood flow through them is amongst the highest recorded in the animal kingdom. Even now there remains much to be known about them, from the ecological level, the extent to which the salt glands are used by different birds in different habitats, for example, right down to secretory mechanism at the cellular and molecular levels.

The story of the discovery of salt glands is in Knut’s autobiography, The Camel’s Nose, published in 1998. His curiosity was aroused when asked to read the proofs of Nobel prize-winning (and soon to be his father-in-law) August Krogh’s book on osmotic regulation. The story actually begins  in 1939. He wrote:

     I learned a great deal from reading the proofs for Krogh's osmoregulation book. One problem that especially intrigued me was how marine birds survive with no fresh water to drink. In search of an answer to this question, I developed methods I could use under primitive conditions, and at the end of the spring term in 1939, after securing permission from the Norwegian authorities to capture birds, I set off for the coast of northern Norway to try to solve the problem. This journey was the first of what would become a long series of field studies around the world, ranging from the Sahara Desert to the Amazon River, seeking answers to problems of how animals survive in hostile environments. 

     In mid-June 1939 I arrived at Röst, a small island in northern Norway, off the Lofoten chain and facing the Arctic Ocean. Millions of auks, puffins, and gulls nest on vertical cliffs that rise out of the ocean beyond Röst. The birds seek their food at sea, and except for rainfall there is no fresh water. Do they drink sea water? I wanted to find out. 

     It was already known how whales and seals can manage. If they drink sea water, the extra salt is excreted by the kidneys. Whale kidneys are powerful and can produce urine more concentrated than sea water. Although no one knows whether whales and seals actually drink sea water, they could readily eliminate the excess salt… 

     Humans have less powerful kidneys than seals and whales. A human castaway at sea who drinks sea water merely hastens the approach of death because the kidneys are unable to excrete the excess salts. Birds seemingly are worse off; their kidneys are even less efficient than humans' in eliminating salts. The problem was to find out if birds get sufficient water in their food, or if they drink sea water and somehow are able to excrete the salts… 

     During the summer I examined skuas, auks, puffins, and kittiwake gulls. The salt concentration in their guts was invariably low and showed no evidence that any of them drank sea water. I also examined five seals shot by a local fisherman; the results were similar. Neither the salt nor magnesium content in the seals' stomachs and intestines suggested that they had drunk sea water. 

     So far I had only negative evidence. The next step was to find out what happens when a bird actually swallows sea water. I captured a few kittiwake gulls and caged them in empty orange crates. They greedily devoured the fish I fed them. Fish doesn't have a high salt content, so I gave one of the birds an ample volume of sea water by stomach tube. If the kidneys excreted the salts, there should be a high salt concentration in the urine. 

     The bird produced copious volumes of urine, but to my amazement the urine had little salt in it. I repeated the experiment with other birds, and again the urine was nearly salt-free. Wondering if my analytical methods were wrong, I tested every step with solutions of known salt content; my methods were 100 percent correct. 

     No matter how much sea water I gave the birds, little salt appeared in the urine. Could it be that the birds retained the salts? If so, the salt concentration in the blood should increase. But my analysis of their blood showed no elevated salt levels. Where was the salt going? I knew it had entered the body, yet I couldn't find it in the urine or in the blood. It seemed that the salt had simply disappeared. 

     At the end of the summer I returned to Copenhagen, disappointed that I had found no solution to the original problem. I was anxious to talk to Dr. P. B. Rehberg, a prominent renal physiologist, who usually gave young scientists excellent advice. However, he said little, and I felt that he perhaps thought I hadn't done a very good job; he didn't even look at my meticulously kept data books. In desperation I suggested that if the salt doesn't come out the rear of the bird, it must somehow come out the front. Rehberg didn't comment… 

     I wanted to tackle this problem again, but the war intervened, and then other projects took all my time. Not until eighteen years later, in 1957 [actually 1956], did I return to the study of marine birds. As I had suggested to Rehberg, a salt load is indeed eliminated from the front end of the bird, as a salty fluid dripping from its beak. Then I understood why I hadn't noticed the phenomenon when I was on Röst. The primitive conditions where I worked, the orange crates and the rough wooden floor, made it difficult to see drops of fluid the birds shook from their beaks. That summer in Norway, I thought the few drops I noticed were no more than a little sea water regurgitated by the bird.

    
The research that led to the discovery of salt glands was done during the summer of 1956 at Mount Desert Island Biological Laboratory (MDIBL), Bar Harbor, Maine, then a gathering place for those studying the kidney and renal excretion during the long vacation, including Knut’s then wife, Bodil, August Krogh’s daughter.

Knut took up the story again in The Camel’s Nose:

     For the study of marine birds I asked two postdoctoral collaborators to join me in Maine: Humio Osaki from Japan and a former classmate of mine from Denmark, Carl Barker Jörgensen. We caught some young cormorants, and to find out what effect sea water has on salt excretion, I gave one of them a liberal amount by stomach tube and placed the bird in a carefully cleaned plastic container. Within a minute or two I made the fastest scientific discovery I ever made. I noticed that the bird, with a quick movement of the head, shook off droplets of fluid that appeared at the tip of its beak. I sampled the clear liquid with a micropipette; it gave a massive precipitate with silver nitrate, revealing a high concentration of chloride. We were astounded, but the result confirmed what I had suggested decades before—that if salts do not come out one end of the bird, they must come out the other. 

     The very salty secretion is produced by glands in the bird's head and drips from the tip of the beak. Thus, if the birds drink sea water, the excess salt is eliminated, leaving a net gain of free water. Whether marine birds in the wild actually drink sea water is a question that is difficult to answer. Nevertheless, much of their food has a salt content high enough to necessitate the elimination of excess salt by the glands we had discovered. For simplicity we decided to call them salt glands. Our discovery received a great deal of attention from physiologists as well as the popular press, for no such gland was known in any animal, and it solved a long-standing problem. 

     I continued these studies over the next two years, both at Duke and in Maine. All marine birds we examined—gulls, pelicans, petrels, eider ducks, and so on—use the same mechanism to excrete excess salt. I had a marvelous collaborator in a Swedish friend, the animal physiologist Ragnar Fänge, who described the detailed anatomy of the salt gland and refined our understanding of its function.

Knut Schmidt-Nielsen working on sea birds at MDIBL
(from here)

Schmidt-Nielsen spent the following summers until 1959 at MDIBL, adding to the previous work. The history also showed that he worked with the MDIBL stalwarts, William L Doyle and Thomas H Maren but they published their salt-gland work without Knut as a co-author. Doyle published the first electron micrographs of the gland. Others there also published on salt glands later, Hubert and Mabel Frings, for example. 

The discovery of salt glands in birds and then in reptiles was just one part of Knut Schmidt-Nielsen’s series of seminal contributions to How Animals Work (the title of one of his books). Obituaries by the late Steven Vogel (1940-2015) and Ewald Weibel can be found here and here.

As Steven Vogel (1940-2015) wrote in Knut’s obituary, in discussing the discovery of salt glands, ‘…the work has taken its place as common knowledge with only rare reference to the seminal reports’. I can only add that, sadly, not only are the references to the seminal reports rare but that the information given on salt glands, particularly in blogs and websites, is so often completely, utterly and completely wrong that it can only be classified as drivel.

At a symposium in Sandbjerg, Denmark to celebrate Knut Schmidt-Nielsen’s 65th birthday in July 1980 there were seven co-authors (out of a possible ten) of his papers on salt glands that were all published between 1957 and 1964 (Ragnar Fänge (1920-1999), Carl Barker Jörgensen (1915-2007) , Maryanne Robinson (Maryanne Robinson Hughes), Arieh Borut, Eugene C. Crawford, Stephen Thesleff, Francis G Carey (1931-1994)). In addition, two of us there (Dennis Bellamy and me) had worked on salt glands later. All the participants and contributors to the proceedings, entitled A Companion to Animal Physiology, received a commemorative medal which show Schmidt-Nielsen’s famous books and the animals with which he was most associated: kangaroo rats, gulls, camels, frogs and snails.

5th International Symposium on Comparative Physiology, Sandbjerg, Denmark, July 1980
To commemorate Knut Schmidt-Nielsen's 65th birthday

And there were Golden Orioles in the trees.


Taylor CR, Johansen K, Bolis L (editors). 1982. A Companion to Animal Physiology: Perspectives. Cambridge: Cambridge University Press

Evans DH. 2015. Marine Physiology Down East: The Story of My Desert Island Biological Laboratory. New York: Springer

*Schmidt-Nielsen K. 1957. Extrarenal excretion of salt in birds. J Elisha Mitchell Scientific Society 73, 235

Bill Sladen (1920-2017): Penguins and Salt Glands

A number obituaries of William Joseph Lambart Sladen who died on 29 May aged 96 have been published in recent weeks. While they all record his pioneering studies on penguins in the Antarctic, his later involvement with migration and conservation projects in the northern hemisphere and his detection of DDT in penguins in the 1960s, they do not mention his involvement with a major scientific discovery of the 1950s which explained how penguins and other birds survive at sea.

Obituary in The Times

This year, marks the 60th anniversary of the announcement of the discovery of salt glands by Knut Schmidt-Nielsen and the publication of an abstract describing the work in Federation Proceedings. A full paper appeared in the American Journal of Physiology in March 1958. A month later a paper in Nature appeared entitled, Nasal salt secretion in the Humboldt Penguin by Schmidt-Nielsen and Sladen, which suggests that the work was done only a short time after that reported in the first paper on the Double-crested Cormorant Phalacrocorax auritus.

Schmidt-Nielsen and Sladen wrote:

In order to establish whether extra-renal salt excretion is of importance in the salt balance of other marine birds, we took advantage of the colony of Humboldt’s penguins (Spheniscus humboldti) in the laboratory of one of us (W.S.). These birds had been caught in the wild six months before, they were doing well in captivity, and were considered to be free of disease. Trial experiments in April 1957 showed that nasal secretion did occur, so the following experiments were performed.

The rest, as they say, is history.

How Schmidt-Nielsen and Sladen got together to do the study I do not know. Since the penguins were kept in Sladen’s lab at Johns Hopkins, I assume the male penguin used was given its salt-loaded fish in Baltimore.

I found this photograph of an Emperor Penguin skull which shows the
supra-orbital position of the nasal salt glands

Sladen by this time had already made his name from studying penguins in the Antarctic. British-born, medically-qualified and working as medical officer as well as biologist for the Falkland Islands Dependency Survey—FIDS—now the British Antarctic Survey, he was sole witness to the horrendous hut fire at Hope Bay in November 1948 that resulted in the death of two members of the survey team. After the fire he spent the next sixteen days alone and out of radio contact, sleeping in a tent, until the main survey party returned. He continued his work on penguins during this time, writing his Oxford doctoral thesis in Charles Elton’s Bureau of Animal Population.

Sladen moved to the U.S.A. in 1956, initially on a research fellowship, and became a U.S. citizen in 1962. He remained based at Johns Hopkins while commuting to the Antarctic and Arctic for his research.

Adélie Penguin - adult and chick
Sladen's early work was on this species at Hope Bay, 9 miles along the
coast from Brown Bluff on the Antarctic Peninsula where I took these
photographs on 26 January 2005.
Salt-gland secretion in this species was described by Donald S Douglas
in the 1960s.

I am taking video of the tens of thousands of Adélie
Penguins at Brown Bluff

Schmidt-Nielsen K, Jörgensen CB, Osaki H. 1957. Secretion of hypertonic solutions in salt glands. Federation Proceedings 16, 113-114

Schmidt-Nielsen K, Jörgensen CB, Osaki H. 1958. Extrarenal salt excretion in birds. American Journal of Physiology 193, 101-107

Schmidt-Nielsen K, Sladen WJL. 1958. Nasal salt secretion in the Humboldt penguin. Nature 181, 1217-1218

Tubenoses and Salt Glands: Up to a Point Mr Packham

Chris Packham, in BBC’s Springwatch Guide to Sea Birds, discussed the tubular extensions to the nostrils of petrels (Procellariiformes). He repeated the common explanation that they serve to remove secretion from the salt glands, adding that otherwise the salt solution would fall on the feathers. They certainly do act as conduits for salt-gland secretion. Shortly after Knut Schmidt-Nielsen discovered salt glands, he wrote an article in 1959 for Scientific American illustrated by a photograph showing salt gland secretion being blown from the tubular nostrils of a petrel.

The late Jim Linzell and I repeated this explanation and reproduced the photograph in our 1975 monograph, Salt Glands in Birds and Reptiles. However, I recall that we both had qualms on whether removal of salt-gland secretion was a real explanation for the evolution of tube noses. Of course, the secretion will come out that way and blowing the secretion out would keep the air channels clear (some species have separate channels in the nostrils for air and secretion). However, other marine and potentially marine birds that have operative salt glands manage perfectly well without tubular extensions. Because we had no other explanation for the adaptation we concluded:

Continuous flight may hamper the flow of fluid from the nostrils because of the current of air over this region and the tubular extensions through which the fluid can be blown by a forced expiration could well act in the way Schmidt-Nielsen suggested.

We did not know then that sea birds have remarkable powers of olfaction and that they use it to detect their prey in the open ocean.

It has been suggested that the tubes serve to direct the current of air to the olfactory epithelium. But is there something special about the tubular arrangement in addition? Does it help in some way to find the direction the odour of prey is coming from while birds fly a zig-zag pattern towards the source? Has anybody looked at the patterns of air flow in the nostrils of birds with and without tubular extensions?

You can see the tubular extensions in this young Murphy's Petrel
(Pterodroma ultima). I photographed this chick on Ducie Atoll in the
Pitcairn Islands on 24 October 2010

So, if I were revising Salt Glands in Birds and Reptiles today, I would point out that salt-gland secretion is blown from the tubular extension to the nares but add that the morphological adaptation is more likely to reflect the survival advantage of an improved efficiency of olfaction rather than of extra-renal excretion.

Schmidt-Nielsen, K. (1959) Salt glands. Scientific American 200, 109-116.

Peaker, M. & Linzell, J.L. (1975). Salt Glands in Birds and Reptiles. Cambridge. Cambridge University Press.

Remarkably, I find our monograph was re-published as a paperback by CUP in 2009 (ISBN:9780521112031) and is available from their website:

http://www.cambridge.org/gb/knowledge/isbn/item5706871/?site_locale=en_GB