Vole Population Crashes: Was there an attempt to suppress a ‘lamarckian’ hypothesis in the 1950s?

Field Vole or Short-tailed Vole
Photograph by Tim Melling

I apologise in advance for this post. In trying to find the answer to an allegation that a paper was suppressed because it proposed a controversial hypothesis, I have to skim the surface of a topic at the heart of ecology. It is a topic that has spilt over into the physiology of ‘stress’ and it is a topic that has been the subject of a great deal of mathematical modelling. I am dealing with just one aspect from a mainly historical perspective but it is an aspect that is at the centre of the problem of factors controlling animal populations and one which provoked an often bitter controversy. The question though is simple: how can fluctuations in the size of populations of voles from year to year be explained?

I knew little of the work of the Bureau of Animal Population which existed at Oxford from 1932 until 1967 under the leadership of Charles Elton¹. What I did know came first from my former colleague at Babraham, the late John Perry², who had been a member of the Bureau in the 1940s, and from his friend H.N. ‘Mick’ Southern³, another stalwart, when the three of us sat together at meetings of the old Zoological Club in the 1970s. Another member, John Clarke⁴, sometimes came to Society for Endocrinology meetings to describe his continuing work on the reproduction of voles. Before that I knew from gossip the battle that went on to bring the Bureau in the zoology department proper because In the mid-1960s interest in the goings on at Oxford was intense. Zoology at Oxford has a well-maintained reputation for internecine warfare and John Phillips⁵ returned to Hong Kong from a short visit to U.K. in 1966 full of stories he had heard of the troubles at Oxford occasioned by the eventually successful attempts of the head of department, J.W.S. Pringle⁶, who had arrived from Cambridge in 1961 determined to change things, to integrate the outlying units, into the zoology department.

A couple of years ago I found that Peter Crowcroft⁷ had written a book on the history of the Bureau, of which he was a former member. As I read it I came across what appeared to be a shocking example of scientific censorship in the early 1950s. I thus became acquainted with the world of voles and of Dennis Chitty⁸ who, after Oxford, was Professor of Zoology in the University of British Columbia. This is what Crowcroft wrote:

When Chitty had analyzed his data from the Lake Vyrnwy population [of the Field Vole, Microtus agrestis] that had been stud­ied continuously from 1936 through 1939, he found himself unable to explain their crash in terms of the classic factors: food, weather, preda­tion, and disease. He came to suppose that overcrowding and its asso­ciated social strife might have caused the high mortality among young voles born when numbers were highest. Adverse effects of overcrowding could also explain the reduced productivity of females subjected to it. That hypothesis would not have caused any raised eyebrows, even in the 1940s. The Lake Vymwy population continued to decline, however, in the next generation, when there was no longer an overcrowded vole society, and when food appeared to be abundant. Chitty felt obliged to offer, as the simplest possible explanation, the existence of an inherited disability: "During the time of their almost complete disappearance in 1938 or 1939 voles were not subjected to any known environmental conditions likely to have caused excessive mortality. The hypothesis is therefore advanced that death was primarily due to adverse conditions to which the parents were subjected in the previous breeding season."       

That suggestion not only caused the eyebrows of authorities in popu­lation matters to go up, it also raised the hairs on the backs of their necks. This smacked of the Lamarckian heresy! Chitty could not get the paper published in the journal of his choice. But Sir Alister Hardy read it objectively, and communicated it to the Royal Society for publication in their Transactions, a most prestigious place. 

Now ‘maternal effects’—an example of which Chitty proposed—are well-known phenomena in many different organisms. They are lamarckian in the sense that a mother (or a father through ‘paternal effects’) can affect the performance of her offspring by pathways not involving a difference in the genes (which would be really lamarckian). Maternal effects, in short, are a form of non-genetic inheritance†.

If what Crowcroft wrote was true, the editors of the journal to which Chitty’s paper was first submitted would indeed have been guilty of suppressing an inconvenient hypothesis. However, Crowcroft made several mistakes in describing Chitty’s work which made me wonder if he had got hold of the wrong end of the stick. The first error was that Sir Alister Hardy did not communicate the paper for publication by the Royal Society. The Fellow who did was the then Professor Peter Medawar⁹. The second was that Crowcroft seemed to confuse this hypothesis of Chitty’s, which involved a maternal effect, with his later hypothesis for the phenomenon of vole cycles which involved genetic selection at different stages of the population cycle. This replacement hypothesis, not the one for a maternal effect, has been termed the ‘Chitty Hypothesis’.

After I read this Crowcroft’s account I began to think that Chitty and the people around his lab (including Crowcroft) had interpreted rejection of his paper because the hypothesis he advanced to explain it was lamarckian, rather than for the multitude of other reasons editors reject papers or suggest parts be rewritten. Crowcroft’s book appeared in 1991. In 1996 Chitty himself wrote a book describing his virtually lifelong interest in the control of animal populations and the disappointments it had caused him.  Chitty made no mention of the paper being rejected because it contained an apparently lamarckian hypothesis but because he had dared to propose a hypothesis at all. He wrote of this episode:

The account of my prewar work would have appeared in the Journal of Ani­mal Ecology if Charles [Elton] and I had not stepped down as editors. But the new editor, H.C. Gilson, took a dim view of the paper and wanted it rewritten. Ten of the pages, he complained, seemed to be largely speculation. “Even if they were not, [he wrote] they would be too general in character to hang on to this paper.” His comments confirmed the doubts I held at the time about the danger of speculating, especially as they were followed by phases such as the following: “All this is mere vague speculation . . . these ex-cathedra statements . . . if you will read the paper critically . . . infuriating to the reader . . . would you make up your mind . . . such indifferent photographs . . . much of interest and value pokes out of the paper like gleams of sun­ shine in places.” 
     I was more than somewhat upset—more than I should have been…This is probably the way most young authors feel when one of their brainchilden has been thrown to the lions of peer review. So it was some time before I could look objectively at the contrast between what I’d writ­ten—“needless to say I shall very gratefully welcome all your criticisms”— and the lack of gratitude I felt when they landed on my desk. 

In short there seemed to be no mention of a particular hypothesis, only that the data did not justify the degree of speculation. Chitty went on to describe the rôle of Medawar in getting the paper published: ‘His opinion of the need to speculate (though not necessarily of how I did it) restored my self-confidence’.

The question remains: would Chitty’s paper rewritten on the lines suggested by the editor of Journal of Animal Ecology have made a better paper than that which appeared largely unchanged in Philosophical Transactions of the Royal Society. I thought I, a non-ecologist, should read it.  And so I did, several times, and found my sympathies lie, 70 years on, with the editor of Journal of Animal Ecology. The style of data presentation alone has changed greatly but even so the paper would have qualified for my late colleague’s description of ‘publishing the contents of his notebook’. However, ‘much of interest and value pokes out of the paper like gleams of sun­ shine in places’ as Gilson wrote. Perhaps Chitty should have grasped the nettle and re-written it in a less discursive style while aggregating the raw data into simpler tables with more statistical analysis. My guess is that Gilson*, as the new editor of Journal of Animal Ecology, was attempting to present ecology as a harder science with crisp analysis and presentation than that conveyed by the previous Elton/Chitty régime.

A fierce critic of Chitty’s interpretation of the data from Lake Vyrnwy was David Lack¹⁰, next door at the Edward Grey Institute of Field Ornithology. Lack was of the view that only three factors can control natural populations: disease; predators or parasites; food shortage. He did not accept that Chitty had eliminated the influence of these factors before producing a hypothesis that crowding and thus ‘strife’—in other words control entirely within the vole population itself—causes the fall in numbers. While Chitty defended his views vigorously, on reading his book I remained unconvinced that he had eliminated the rôle of ground predators like stoats and weasels or that tuberculosis, which was present, might have been more important in the population declines than the evidence then suggested.

If, on the other hand, the external factors of Lack really can be eliminated as an explanation, which Chitty continued to contend, and having read something of the recent thinking on explanations of cycles in vole populations, there seems to be the view that Chitty’s original idea of maternal effects brought on by crowding might provide the answer rather than his ‘Chitty Hypothesis’ based on changes in selection and gene frequency.

In conclusion, I have not been able to confirm Crowcroft’s view that Chitty’s paper was rejected by the editor of Journal of Animal Ecology because it ‘smacked of the lamarckian heresy’. It is true that rejection on those grounds could have been hidden in the criticism of ‘speculation’ but having read the paper I can see why the editor acted as he did; he may not have objected to a particular hypothesis but to any hypothesis being advanced from what he, or possibly a referee advising him, saw as incomplete or inadequate data.

Finally, Lake Vrnwy, an artificial reservoir in North Wales which supplies Liverpool with tap water, is well-known to those who watch Springwatch on BBC television. The surrounding land is managed by the RSPB and in case any readers wonder where exactly the vole surveys of the late 1930s were done, I have drawn them on the map produced for visitors to the reserve. The habitat is though probably not suitable for Field Voles. At the time of the studies trees had been planted for forestry but the open nature of the ground remained vole friendly. That is probably not the case now but never having been to Lake Vrnwy I do not know.

The RSPB current map with the study areas from the 1930s marked in RED

     

After reading about vole cycles and the lack of any settled view on their cause I was left feeling that a long-term study should be done in a suitable habitat, applying all the knowledge of how to do such research that has accumulated over 80 years. While the same areas around Lake Vrnwy may not be suitable, why not repeat the studies elsewhere?

Dennis Chitty
from obituary by Charles J Krebs
for the
Royal Society of Canada

from Acta Theriologica 42, 1997

*The editor was Hugh Cary Gilson (1910-2000) a freshwater biologist who from 1946 to 1973 was Director of the Freshwater Biological Association.

†A good definition of maternal effects was provided by Mather & Jinks in 1970: Maternal effects arise where the mother makes a contribution to the phenotype of her progeny over and above that which results from the genes she contributes to the zygote. 

1.Charles Sutherland Elton FRS, 1900-1991

2.John Sherwood Perry, 1917-2010

3.Henry Neville "Mick" Southern, 1908-1986

4.John Rigarlsford Clarke, ca 1925-2010

5.John Guest Phillips FRS, 1933-1987

6.John William Sutton Pringle FRS, 1912-1982

7.William Peter Crowcroft, 1922-1996

8.Dennis Hubert Chitty, 1912-2010

9.Peter Brian Medawar OM FRS, 1915-1987

10.David Lambert Lack FRS, 1910-1973

Chitty D. 1952. Mortality among voles (Microtus agrestis) at Lake Vrynwy, Montgomeryshire in 1936-9. Philosophical Transactions of the Royal Society B 236, 505-552.

Chitty D. 1996. Do Lemmings Commit Suicide. New York: Oxford University Press.

Crowcroft P. 1991. Elton’s Ecologists. Chicago: University of Chicago Press.

The Kitching-Ebling split, Lough Ine (Hyne) and Reflections on a Summer Sea

Scientific divorces, whether of long-term collaborators, scientist and technician or scientist and past research student,  are horrendous—both to both the parties involved and to onlookers and friends. The reasons are often obscure and may take years to come to the boil. Jealousy, perceived slights, perceptions of unequal work load can all come into the mix.

One of the saddest cases was that of Jack Kitching* and John Ebling†. Their exploits each summer in exploring the ecology of Lough Ine, or Hyne as it is now known, a sea-loch in Ireland, with zoology students initially from Bristol and then, when Kitching moved, from the University of East Anglia, was known more widely and it was a constant feature in both of their lives from 1937 and 1938. Kitching was then a young lecturer and Ebling an undergraduate. They published many papers together and pioneered an experimental approach to ecology. Ebling moved from Bristol, had a short spell in Hull and then established himself in Sheffield where he rose through the ranks to the second professorship in zoology—then a vary rare promotion. Throughout, he headed the logistics of getting the equipment and people to Ireland each year and organising the supplies of food and alcohol. There seems no doubt, though, that Kitching regarded Loch Ine as his show and as his territory.

The Kitching and Ebling Summer Show at Loch Ine was captured superbly by Trevor Norton’s 2001 book, Reflections on a Summer Sea. He began it by quoting a letter he had written to Jack Kitching in 1994:

I have begun to write the story of Lough Ine. I want to tell of the stunning scenery and terrible history of the place, the myth and the magic, and to recapture all the fun and excitement we had in those summers when we waded and dived in the lough. Perhaps I can convey the wonder I felt when I first came to Lough Ine in the 1960s, and maybe slip in a bit of marine biology too…

and continued:

This is the story of the menagerie of eccentric and talented ecologists who, as a hobby, established a privately owned field laboratory in south-west Ireland and took part in one of the most unlikely projects in the history of marine biology.

I heard of the Kitching-Ebling split around 1987 from John Ebling himself. I found him or, more correctly, heard him, holding forth in the Staff Club at Sheffield in, I think 1987 or ’88. I left my host and went over to talk to him. In our student years in the 1960s, John had waxed lyrical about the summers on Lough Ine and so I asked him if he was still going. ‘No’, was the reply and he went on to explain that Kitching had cut all ties with him some years earlier and that he was no longer welcome. He was clearly distressed and utterly bewildered about the whole affair. We moved on to pleasanter matters and I left him to resume his conversation. That was the last time I saw him.

Trevor Norton saw at close hand the whole relationship between Kitching and Ebling and the eventual break up. The immediate cause appeared to be Kitching’s proprietorial attitude to Lough Ine and his attempting to hang on in research after his retirement against a background of tightening funding and lack of recognition of the importance of work there. It would also seem that Kitching came to resent his former student’s success in other fields, for John was at home with errant polychaetes, moulting patterns of mammals, hormonal effects on the skin, clinical dermatology and the effects of cosmetics.

So while it seems pretty clear that John Ebling was the injured party, as was Trevor Norton himself when he disagreed with Kitching on the direction the research should take, there did come a sort of and rather sad rapprochement. Trevor described a symposium in Cork in 1990 on the research at Lough Ine. Kitching and Ebling were both invited:

Although it was a relief to John to have an invitation and a chance to visit the lough, he was nervous about meeting Jack again. He needn’t have been, for Jack was no longer formidable. John was a ebullient as ever, but a stroke had stolen Jack’s vigour. He looked and sounded frail, a ghost of his old self. I feared his lecture might be a disaster, but on stage he rose to the occasion and spoke well. I saw John helping him across the road. They were chatting, perhaps about old times.

There Trevor left it and so I was delighted to find that a book of photographs illustrating the history of the people who made Lough Ine famous—now the subject of over 450 scientific publications had been published in 2011. Many of the photographs are Trevor Norton’s but it covers work from 1885, when the first studies of the lough were made, until 2010. When I received my copy I was delighted to recognise people I had met and worked alongside in parallel universes without knowing they had spent one or more summers there.

I cannot help but end with a John Ebling story. Trevor Norton explains how Jack Kitching disapproved of John’s ribald sense of humour especially in front of the students, “these tender plants”. My abiding memory is of Venice at Easter 1964. We had arrived by bus from Rovinj where we were being exposed to a marine biology field trip (Lough Ine lite is the best description I can think of with hindsight). The bus journey had taken several hours and we were dropped off at a vaporetto-stop where we found public lavatories before heading for St Mark’s Square. Italy at that time had the lira and inflation had led to massive numbers of lira being needed for everything. The relatively small number of men and the larger number of women lined up with John heading the queue (student prostates were smaller and bladders possibly bigger) to pay and enter. After several minutes inside he re-appeared. ‘I am reminded of that old rhyme written behind the door in gents’ lavatories’, he said. And continued:

Here I sit, broken hearted, 

Paid two-thousand lira and only farted.

I cannot enter a public lavatory anywhere in Europe without repeating that incantation. Kitching would not have been amused.

These are photographs from Terri Kearney's superb book of photographs:

Jack Kitching on his first visit in 1938

Ebling and Kitching on the front row at the conference in Cork when they met again in 1990

*John (“Jack”) Alwyne Kitching OBE FRS (1908-1996)
†Francis John Govier Ebling (1918-1992)

Norton T. 2001. Reflections on a Summer Sea. Century (paperback 2002, Arrow Books)

Kearney T. 2011. Lough Hyne. The Marine Researchers - in Pictures. Skibereen Heritage Centre. Obtainable from here.