Part 2. The Beginnings of the Ecosystem Concept Proper

Charles Elton and Food Webs
No doubt about it, Charles Elton was a genius in the true sense of the word. He read, and understood, Charles Darwin's Origin of the Species when he was only 16! What were you doing when you were that age? He entered Oxford just after WWI, and studied zoology with the great Julian Huxley, who was making his reputation as one of the foremost authorities on bird behavior. In addition, while at Oxford, he had the opportunity to go on several expeditions to the arctic, which introduced Elton to field research.

At this time, most of the community ecology work going on was done by botanists, and little was done by zoologists. This type of work held little appeal for the precocious young researcher, and he decided early on to pursue the relationships animals had with one another within the context of the communities as delineated by the botanically inclined ecologists. What is remarkable is that when only 26, he published his first book, Animal Ecology, in 1927. Wrote Elton, "Food is the burning question in animal society, and the whole structure and activities of the community are dependent upon questions of food supply."

Elton championed the concept of the niche, the role that a species played in its community. He viewed this as a way to structure future research, because the niche concept allowed ecologists to make predictions about the structure of animal communities. In addition, it could be used as a comparator between different communities, i.e., did the same feeding relationships, or niches, occur in different communities? Why or why not? For example, he showed that the communities around Oxford contained birds that consumed small mammals, such as mice and shrews, and that in oak forests, tawny owls were the birds of prey, while in grasslands, kestrels fulfilled this niche.

Elton began to develop the concept of a food chain, that one organism eat another, who in turn is eaten by another, and so on. He extended this concept to be more than just a diagram of who eats who, but suggested that the feeding relationships so diagramed constituted the fundamental processes by which the community itself functioned. Food chains began at the bottom with plants, and then herbivores who ate the plants. Their abundances were set in part by the availability of plants. Next were carnivores that preyed upon the herbivores. Their abundances were governed by how many herbivores there were, and so on. But as one moved up the food chain, there were fewer and fewer carnivores, and ultimately the chain played out. Elton noted, as others had before him, that it often extended for only 4-5 links before there would not be enough resources to support another carnivore. Elton called this the pyramid of numbers.

However, the world is not so linear or simple. Elton quickly realized that certain organisms short-circuited this simple scheme, such as parasites, or that animals changed their feeding habits as they grew, and he adopted the concept of a food cycle, known today as a food web.

Elton argued that in a given habitat, there was a fixed availability of food, and that, in turn, regulated animal population abundances. As the food supply varied by any number of causes, that, in turn, instigated changes in animal abundances, and populations tended to fluctuate about, rather than to maintain constancy in numbers. As you can see, Elton was building on what Forbes, 40 years earlier, had called "the community of interest" among predator and prey (Hagen, pg. 54). At the beginning stages of his research, which he carried on around Oxford for over 20 years, he wrote: "The food-relations of animals are extremely complicated and form a closely and intricately woven fabric - so elaborate that it is usually quite impossible to predict the precise effects of twitching one thread in the fabric. Simple treatment of the subject makes it possible to obtain a glimmering of the principles which underlie the superficial complication, although it must be clearly recognized that we know at present remarkably little about the whole matter."

Surely this represents sophisticated thinking at an early stage in his career, and shows his hope that by studying food webs, a greater understanding of how communities operate can be elucidated. Many of his ideas sprang from his arctic trips, where he was able to see through the complexities, because of the relatively simple nature of the communities up there. As Hagen and others have pointed out, a central theme running through Elton's work is that communities are highly integrated, self-regulating systems. This is set much of the stage for future ecosystem ecologists, and became a framework under which the study of energy flows began.

Elton also acknowledged the importance of certain key species, today known as keystone species, who, if subjected to great changes in population, have undue influence on the community. For example, the removal of predators such as wolves and coyotes can greatly upset the deer population, as happened at the Kaibab Plateau, in Arizona.

But he was quick to point out that communities were not stable, equilibrium states, but rather, that all the interactions among species resulted in constant adjustments to populations sizes. The so-called balance of nature did not exist: "The 'balance of nature' does not exist and perhaps never has existed. The numbers of wild animals are constantly varying to a greater or less extent, and the variations are usually irregular in period and always irregular in amplitude."

Thus, Elton's legacy was that he freed the concept of the community from the rigid thinking of Clements, and Elton pursued the idea of community from a much more abstract point of view. His concepts of the food web, the niche, and self-regulation became the foci for later studies on trophic dynamics, as we will now document.
 

G. Evelyn Hutchinson - An Original Thinker
I remember G. Evelyn Hutchinson as a small, frail man, with stooped shoulders, and bags under his eyes. Of course, at the time, Hutchinson was in his late 70's or early 80's. However, his appearance was no reflection of the bright mind that lurked inside his head, or of the tremendous influence he had on ecology in the 20^th century. Hutchinson spanned the time between the end of the Victorian age, right up to modern day ecology. He knew Francis Darwin, the famous son of Charles Darwin, and he was associated with some of the seminal papers and schools of thought regarding ecology in this century, including perhaps the most famous ecological paper ever written, Lindemann's The trophic-dynamic aspect of ecology, published in 1942 in Ecology. More about that later. So why was Hutchinson so influential?

Hutchinson was Elton's junior by two years, so the two ecologists rose to prominence at nearly the same time. While Hutchinson, who was raised in England, was a young instructor in South Africa at the University of Witwatersrand, he read Elton's book Animal Ecology, and was deeply impressed by it. Wrote Hutchinson, "it proved a stimulus by showing me that what I wanted to do in biology was indeed a significant part of the science." However, Hutchinson approached his science with a much more quantitative zeal, in contrast to Elton, who tended to avoid highly mathematical models. And though Hutchinson was not solely a theorist, but rather, combined both empirical and theoretical work, he was much better at abstraction and model building. Hutchinson was one of the first ecologists to create "black boxes" to model the inputs and outputs of materials, a precursor to later modeling by systems ecologists. Thus, Hutchinson set the stage for how ecology, particularly ecosystem ecology, was to develop.

Hutchinson moved from South Africa to Yale University in 1928, and was one of the only ecologists in the zoology department at that time. Freed from working within an established group, he was able to pursue what some thought were highly eclectic studies, but which turned out to be highly influential later on. A widely trained biologist, Hutchinson also had interests in chemistry and geology, traits that proved invaluable to his later research in biogeochemistry. By circumstance, he was friends with Viktor Goldschmidt, a geochemist who was a friend of his father's, and Vladimir I. Vernadsky, a theoretical ecologist, whose son, a historian at Yale, introduced Hutchinson to his father's writings. In fact, Vernadsky and Hutchinson later collaborated to translate Vladimir Vernadsky's writings into English, to make them available to a broader audience.

Vernadsky was among the first to propose a concept of the biosphere, that life existed only within this thin layer around the earth. Although he didn't originate this concept, he did emphasize how life moved materials around the globe in great cycles, and this was indeed breaking new ground. He believed that geochemistry was in large part, biogeochemistry, and can be regarded as the founding figure in nutrient cycling research.

As Hutchinson pondered global geochemical cycles, he came to realize that to fully understand them, he would need to study cycling on a much more restricted and controlled scale. He chose to work in a lake ecosystem near Yale, called Linsley Pond. He used Linsley Pond as a microcosm for how global geochemical cycles worked. Linsley Pond is a small nutrient-rich (eutrophic) lake of about 25 acres on the outskirts of New Haven, CT, where Yale is located. Its maximum depth is only about 50 feet. Starting in 1935, Hutchinson and his students began what amounted to a 20 year study of the ecology of this lake, particularly its nutrient cycling and water chemistry. One of Hutchinson's early Ph.D. students, Edward S. Deevey, who later became famous for creating the three survivorship curves familiar to all who take introductory ecology, began drilling cores in the sediments of the lake. He and Hutchinson found that they could resurrect the history of the area all the way back to the times of the glaciers by analyzing the contents of the sediment cores they extracted. They found that early on, the lake was highly unproductive (as a recently formed glacial lake should be). Then, as materials flowed in from surrounding areas, bringing in necessary nutrients like N and P, productivity increased (based on increased numbers of organisms and organic matter content). But it was not linear. When a limiting nutrient like P reached a particular level, it freed organisms from their previous constraints, and productivity took off exponentially. But this lasted only a short (geologically speaking) time, and then productivity essentially leveled off, once the lake was eutrophic. Hutchinson called this trophic equilibrium.

Hutchinson likened the period of growth in productivity to that of an organism, while realizing that the lake was not an organism. He showed that early successional organisms could modify the lake so that it became more suitable for other organisms, who in turn modified it further. While it might be tempting to suggest that Hutchinson and Deevey were simply reifying Clements' organismal concept, it is more likely that these analogies arose from Hutchinson's background as an embryologist (when he was brought to Yale he was asked to embryology), and that these analogies arose from his experience with how organisms developed through time. By the early 1940's, Hutchinson had created a new way of studying aquatic systems, limnology, and was attracting some of the best and brightest minds in the field. Hutchinson would later embark on a several decades writing effort, culminating in several volumes on limnology that are regarded today as classics in the field.

As Hutchinson's work in limnology developed, he expanded his interests to problems in general ecology. Hutchinson thought that ecology encompassed a variety of subjects, ranging from the biological to the purely physical, and that a biogeochemical approach was one way to unify these two poles of research, coupled with a demographic approach, which concentrated on population dynamics and the factors regulating them. Hutchinson also regarded ecological systems as composed of parts that had self-regulation and feedback mechanisms, something which arose out of his interest in cybernetics, or the study of systems. This meant that most processes could be studied using mathematical modeling. In 1946, Hutchinson put these synthesized these ideas in a landmark paper, Circular Causal Systems in Ecology, presented at a symposium on Teleological Mechanisms, which was designed to investigate cybernetics. Present at this meeting were such luminaries as John von Neumann, and Norbert Wiener, to name but a few.

Hutchinson took the famous Pearl-Verhulst equation of exponential growth:
 

dN/dT = Nb(K-N)/K
 

where K is what Hutchinson called the saturation capacity, known today as the carrying capacity. b is the rate of intrinsic increase, in Hutchinson's notation. Although the (K-N)/K term does not explicitly explain how a population slows its growth rate down, Hutchinson said that it did represent a feedback mechanism in the community, and that this was a universal principle in all ecological systems. It thus provided a theoretical bridge between the physical and biological aspects of a community.

Hutchinson later expanded on this to include time lags, which provided for the oscillations in populations that many scientists predicted from these equations should occur in nature. In a sense, he was attempting to put in formal mathematical terms, some of the natural history ideas of Elton. He also incorporated Lotka and Volterra's predator-prey equations in his paper, and pushed forth the idea that natural selection would act to minimize oscillations in predatory and prey populations over evolutionary time, which is why oscillations were difficult to find in the field.

These same equations could also be used to model biogeochemical cycling. In fact, Hutchinson used them in one section of his paper to argue that human inputs of CO₂ to the atmosphere would not cause the atmospheric concentrations of CO₂ to increase, reasoning that as more CO₂ entered the atmosphere, feedback mechanisms would kick in, such as increased photosynthesis, and diffusion in the oceans, which would keep the concentrations from rising. Of course today we know he was dead wrong on this.

When Hutchinson retired in 1971, he had advised 40 Ph.D. students, and he had authored over 200 publications, many of them classics in ecological writing. In his later years, when I met him, he was finishing up his book on Population Ecology, which I have here. This is a testament to old style writing, and devotion to historical context, as nearly 1/3 of the text is footnotes expanding on particular subjects in the main text. If you haven't read this, or seen it, you should peruse through it. While I was at Yale, he would periodically come in and lecture from the chapters, and ask us for comment. I was most impressed to be in his presence.

As much as for his science, Hutchinson is known for the students he produced. I've already mentioned Deevey, but others included Gordon Riley, his first student, Howard Odum, and Frederick Smith. Perhaps known is more famous than Howard Odum, about whom we will speak later. However, Hutchinson's approach, a combination of mathematical theorizing, systems analysis, and empirical observations, was not without its detractors. The other great school of limnology, centered in Wisconsin and headed by the mercurial Chancey Juday, thought little of Hutchinson's work. Juday even wrote once:
 

"The Yale school of mathematical-limnologists is having a high time displaying their mathematical abilities. The interesting part about it is that they are applying mathematical formulae used in sub-atomic physics where all the forces are presumably uniform to limnological problems where there are all sorts of un-uniform factors involved....Apparently they do not have the brains enough to see the point in the two very different situations....In short time I shall expect them to tell all about a lake thermally and chemically just by sticking one, perhaps two, fingers into the water, then go into a mathematical trance and figure out all of its biological characteristics.   As the next stage in their evolution they will probably be able to give a lake an "absent treatment" similar to a spiritualist, so it will not be necessary to visit a lake at all in order to get its complete chemical, physical, and biological history."

Hutchinson's lab retorted that Juday's lab was capable of making ten thousand measurements without coming up with a single idea (Hagen pg. 96)! This antagonism, as we shall see below, nearly derailed publication of Lindemann's epochal paper, and provides a bit of la joie de vivre in our study of the history of ecology.
 

Arthur George Tansley - Inventor of the Term 'Ecosystem'
Although both Elton and Hutchinson both worked in what we would now call the field of ecosystem ecology, neither used that term very much, if at all. Had they come up with it, they most likely would have appropriated it to describe their research, but in fact, the term ecosystem was derived in 1935 by Sir Arthur Tansley, a botanist at Cambridge University.

Tansley presented the concept in a paper titled, "The Use and Abuse of Vegetational Concepts and Terms" in Ecology in 1935. Wrote Tansley:

"But the more fundamental conception is, as it seems to me, the whole system (in the sense of physics), including not only the organism-complex, but also the whole complex of physical factors forming what we call the environment of the biome - the habitat factors in the widest sense.  It is the systems so formed which, from the point of view of the ecologist, are the basic units of nature on the face of the earth.  These ecosystems, as we may call them, are of the most various kinds and sizes. They form one category of the multitudinous physical systems of the universe, which range from the universe as a whole down to the atom."

What Tansley proposed in his ecosystem concept can be broken down into three major parts: 1) it is an element in a hierarchy of physical systems, 2) it is the basic unit of ecology, and 3) composed of both the organism-complex and the physical-environmental complex. These ideas continue to be key concepts today in ecosystem ecology.

Tansley, born in 1871 to a businessman, attended Trinity College in Cambridge in 1890, where he read widely in botany, zoology and physiology, along with geology. His interest in botany led him into ecological work, as did experiences on several field trips, including visits to Malay and Ceylon. In 1902, he started the botanical journal, New Phytologist, which I have published in, and which each year publishes the Tansley Reviews, named after its founder, and who served as editor for nearly 20 years. When he retired in 1937, he was the most influential ecologist in all of Britain.

Tansley called for, and got, a survey of the vegetation the British Isles in 1904, and when he became involved in ecology, saw the need to create a society for these researchers. Thus, in 1913 he founded the first ecological society in the world, The British Ecological Society. In 1915 he was made a fellow of the Royal Society, and knighted in 1950.

What concerns us today is how Tansley came to write his article in which he coined the term ecosystem. The impetus was an invitation to write an article in honor of Henry Cowles, whom Tansley admired. As Tansley said of Cowles, "During the first decade of this century indeed Cowles did far more than any one else to create and to increase our knowledge of succession and to deduce its general laws."

However, the stimulus to write what he did came, it appears, from his dissatisfaction with a series of articles by a South African ecologist, John Phillips, who wrote on biotic communities, succession, and the climax and super-organism concept. Phillips was enamored of Clements' views and ideologies, and hammered that home in his series of articles. This appears to have incensed Tansley, who, although he corresponded with Clements, and was appreciative of Clements' body of work, disagreed with him over the superorganism concept. That Phillips was strongly endorsing Clements' views outraged Tansley, and he penned the article referred to above. Tansley said, "Phillips' articles remind one irresistibly of the exposition of a creed - of a closed system of religious or philosophical dogma." There thus seemed justification for Tansley's acerbic claim that Phillips' articles rested on faith, since according to Phillips, if the community was an organism, it had to develop to a single, adult, form (Hagen pg. 84).

Phillips took some of his philosophy from the philosopher-general, and later Prime Minister of South Africa, Jan Christian Smuts, a contemporary and associate, who wrote extensively on a holistic philosophy. In 1926 Smuts published a book titled Holism and Evolution, wherein he called the synthesis of matter, life, and mind, based on science, holism.

As he wrote in his book:

"Taking a plant or animal as a type of a whole, we notice the fundamental holistic character as a unity of parts which is so close and intense as to be more than the sum of its parts: which not only gives a particular conformation or structure to the parts but so relates and determines them in their synthesis that their functions are altered; the synthesis affects and determines the parts, so that they fucntion toward the 'whole'; and the whole and the parts
therefore reciprocally influence and determine each other, and appear more or less to merge their individual characters."

As noted by Golley (A History of the Ecosystem Concept in Ecology, pg. 26) it was Phillips that extended Smuts' ideas on 'wholes' and holism into ecological thought, and that were it not for Phillips, most ecologists would never have heard of Smuts or his philosophy.

To assist us with understanding Tansley's view on the subject, we need to understand that at this time, there was much debate about reductionism (reducing a phenomenon to its constituent parts, and analysing the phenomenon by these parts) and holism (which attempts to understand how a system works by figuring out how the parts interact to create the whole, i.e., a top-down approach). And Tansley had carried on a warm correspondence with Clements over the years, and especially liked his work on succession. However, Tansley later wrote, "I...believe the analogy with the organism to be legitimate if it is not pushed too far, and especially if we abstain from making illegitimate deductions." As Hagen points out (pg. 82) for Clements, succession was not simply analogous to ontogeny, it was ontogeny.

Tansley was seeking to create a middle ground, to bring together these two polar approaches to science, and the ecosystem concept was his attempt at doing so. Tansley's concept of the ecosystem stressed the interplay between the organic world, and the physical environment about it, and that these interactions resulted in the ecosystem. He rejected Phillips' and Clements' arguments that communities were superorganisms, and in later life, this led to his distancing himself from Clements. Interestingly, Tansley never used the ecosystem concept in his own research, preferring instead to do administrative work, and field biology, even delving into psychology for a time with Freud.
 

Raymond Lindemann - Genius Cut Short
Raymond Lindemann was a bright student from Minnesota. He attended Park College in Missouri as an undergraduate, and expressed a desire to become a scientist at an early age. After graduating from Park College, he pursued further study with the limnologist Samuel Eddy, at the University of Minnesota. Although Eddy was a competent scientist, it appears that the major influence on Lindemann was W.S. Cooper, a student of Cowles, who taught botany at the university. Cooper provided Lindemann with an historical background in ecology and with the current arguments in ecology that were swirling among ecologists. By the time he finished his doctorate, Lindemann was fully aware not only of limnology, but the major philosophical points of plant ecology, including those important subjects of succession and climax communities.

Lindemann then came to Hutchinson's laboratory in September of 1941 on a postdoctoral fellowship. Although he unexpectedly died the following June, he and Hutchinson were able to publish the trophic-dynamic paper, with a large contribution by Hutchinson several months after Lindemann died. The paper didn't have an easy gestation, as it was originally rejected when submitted to Ecology. The two editors who rejected it were Juday, and an associate Paul Welch. We've already seen the antagonism Juday had for the Hutchinsonian approach, so this is not surprising. However, Hutchinson wrote a strong rebuttal to the rejection and petitioned the editor, Thomas Park (famous for his Tribolium competition studies) to reconsider it. Park sent it out to yet a third reviewer, Warder Clyde Allee (famous animal ecologist). Allee too only gave it a warm endorsement. Juday and Welch both wrote back that it was still an unacceptable paper, but after mulling it over for a while, Park decided to publish it, with the admonition that:

"Time is a greater sifter of these matters and it alone will judge the question."

During the negotiations over the paper, Lindemann suffered an attack of jaundice (probably hepatitis) and died very soon after (June 15). The paper appeared four months later.

The intitial reaction to the paper ranged from luke warm, to dismay, to acceptance. Much of the resistance to the ideas contained therein most likely stemmed from the heavy emphasis on the mathematics, which was quite different from most ecology papers (and not unlike the reason Mendel's work was ignored for nearly 30 years!). In addition, Hutchinson's research group, while growing and influential, did not yet equal that of their rival, Juday, and hence many were reluctant to shift camps, so to speak. In addition, Lindemann's paper attempted to draw sweeping generalizations from a limited amount of data. If anything, Juday's work had shown that the variability in community processes and chemistry varied widely from lake to lake, and thus his group was reluctant to generalize from such a small database.

In addition, Juday's work tended to be "bottoms-up" research, while Hutchinson's was more "top-down". However, even Lindemann knew he was stretching it a bit, as evident in a letter he wrote to his former mentor, Cooper: "I have a feeling, though, that at least some of these ideas are piquing enough to start some people making ecological studies on the basis of productivity and efficiency, and that would be quite gratifying even though some of the proposed 'principles' turn out to be wrong."

The Trophic-Dynamic Paper - What Does it Say?
During the conceptualization of his Ph.D. thesis, Lindemann concluded that the lake was an ecosystem in the sense that Tansley meant it to be used. Lindemann felt he had to conceptualize the myriad interactions occurring in the lake in order to make sense of the entire system. As a start, he grouped organisms that lived in the sediments into one group called 'ooze'. See the diagram in your book on page 51, Golley. On one side of the diagram was a flow structure that included the plankton, while on the other side was one that included the pond weeds. All parts of the biota were linked by the ooze. Of importance was the explicit links that Lindemann made between the living and non-living parts of the system. It's interesting at this point to note that others had drawn similar relationships, but Lindemann then took it one step further. He focused on the food cycle in the lake, which allowed him to relate various organisms to each other and to the non-living parts of the lake. He grouped species into guilds, based on their feeding habits. Then, he converted food groups into energy units to make everything comparable across the system. Finally, Lindemann took this unique approach and applied it to the subject of succession, which Hutchinson and Deevey had been working on. A few years earlier, Lindemann had met and discussed some of these ideas with Deevey at a hydrology meeting, and in fact, it was Deevey who suggested Lindemann apply and come to work with Hutchinson!

By converting the biomass of all the species in the lake, Lindemann could calculate the movement of energy units within and among the various feeding groups in the lake. Using numerical data from Juday's work in Wisconsin, he assigned the appropriate values to his species in the lake he was working on, Cedar Bog Lake near the University of Minnesota. This was a small lake, with a total shoreline of only 500 meters. Lindemann then calculated the energy transfer among three major groupings, producers, primary consumes, and secondary consumers. The data showed that about 10% of the production by producers ends up in the production of primary consumers, and about 19% of primary production ended up in the production of secondary consumers. These data formed the basis for the now famous dictum that from trophic level to trophic level, about 10% of the energy is transferred, with the rest lost as metabolic waste heat, or indigestible food materials. This part of his work became the last chapter of his thesis.

When Lindemann arrived at Yale, he discovered that Hutchinson had independently come to some of these same conclusions. The two collaborated on the paper in the short time they had together, and Hutchinson is known to have substantially added and altered the tone of the paper to meld the theorizing of Hutchinson into that of Lindemann's. In conclusion, as pointed out by Golley (pg. 55) there were three novel results that came out of this paper: "1) the energy of the contributing level a is greater than that of the receiving level b, 2) that respiratory loss is higher at the higher trophic levels, and 3) that consumers at higher trophic levels are more efficient in energy transfer than those at lower levels. These latter two conclusions were references to the process of succession, i.e., that productivity and efficiency increase in early succession, and that consumer efficiencies increase during succession."

Lindemann's paper set the stage for the next generation of ecologists, and after a hiatus due to WWII, the research agenda that he allowed to become a reality took shape.