Part 1. Nature in Equilibrium and then Not!
The history of ecosystem ecology can be extended back to the mid 1800's to the time of Charles Darwin. According to Joel Hagen (An Entangled Bank, 1992) Darwin was faced with contradictory viewpoints about nature. On the one hand, he viewed life as "an entangled bank", full of life forms interacting, yet somehow the bank persisted, it was stable from all outward appearances. This was the deterministic Victorian viewpoint, of a clockwork universe, that despite all the interactions among the organisms, the basic big picture was one of order and persistence, nature operating as it was intended.
The opposing idea was that nature was, as Alfred Lord Tennyson put it, "nature, red in tooth and claw"(In Memoriam, 1850: http://www.chass.utoronto.ca/~ian/inmemor.htm: see verse LVI for quote). That is, organisms fought and competed with one another, with the victors leaving their offspring to the next generation, and with little or no compassion for either the winners or losers. But if such apparent chaos was going on within the seemingly placid bank, how could the entire community of organisms give off the appearance of stability? And how could it persist through time?
Thus one of ecologies first dichotomies was set up: was the ecology
controlled by forces acting up from smaller parts,
i.e., a bottoms-up approach, or, were there factors at work
imposing order on all the parts, factors not apparent from studying the
individual organisms, i.e., a top-down approach?
This set the intellectual framework upon which much later research was
based. The move from a view that nature was stable and in equilibrium to
a realization that, in fact, much of nature is always in dis-equilibrium,
and constantly changing, set up intellectual tensions (Hagen, pg. 3) and
pre-determined the research agenda for future generations of ecologists.
The Influence of Herbert Spencer
Shortly after the publication of Darwin's Origin of Species, a social philosopher in America, Herbert Spencer, began to write that the law of natural selection might act on many levels, from physiological to social. As Hagen (pg. 4) writes, Spencer saw a close parallel between the physiological body and the body politic. His famous 1860 essay on human society (The Social Organism) owed its origins to a mode of thought called organic analogy, which by use of analogies, attempted to show how higher level phenomena could be explained by referencing how individual organisms behaved. For example, organisms were born, grew and increased in complexity through differentiation, the latter factor distinguishing living from non-living things, i.e., crystals. Organisms also exhibited division of labor among the parts, and they showed part/whole relationships, that is, each part had its functions, while together all the parts imparted properties not easily predicted from the study of the individual parts themselves. This is the so-called emergent properties schema that Eugene Odum, one of this century's foremost ecologists promulgated in his influential textbook, Fundamentals of Ecology, which came out in the early 1950s. Institutions, even social ones, showed what Spencer considered similar modes of behavior - societies were born, they developed, and they often died. This way of thinking, by use of analogy, was very common in the 1800s. Whether correct or not (and most argue today that these analogies are fatally flawed) historians are quick to suggest that Spencer had an enormous influence on future ecologists, and the way they framed their theories, many of which had organic references and analogies in them. Thus was formed the first glimmerings of the conceptual framework in which ecology was to develop.
Spencer's organic analogy became a framework for framing questions about ecology - interdependence of parts, part/whole relationships, development through time, and so on. And in this sense, some people think Spencer's ideas were crucial to how ecology itself developed over the next several decades, and in fact, through this century. As an example of some of his analogies, he compared telegraph lines to nerves, railroad systems to arteries, and money to red blood cells. But even he was smart enough to know that the analogy was not perfect. Wrote Spencer, in criticism of Plato and Hobbes:
"Both thinkers assume that the organization of a society is comparable, not simply to the organization of a living body in general, but to the organization of the human body in particular. There is no warrant whatever for assuming this."
Another problem, alluded to in Spencer's, The Social Organism, was the ambiguous relationship (as Hagen puts it, pg. 6) between competition and stability. Spencer felt that strong competition bred stability in society, by weeding out weak and poor companies and ideas, and this in turn, strengthened society as a whole. But of course, this did not turn out to be the case all the time. Unregulated competition sometimes led to economic strife (railroads, communications) and thus the analogy broke down. But its import for ecology held sway for many years, resurfacing in the middle to later decade of this century as the great debate between diversity and stability - did species diversity enhance stability, or reduce it, or did stability permit diversity?
What was the immediate legacy of Spencer's writings? To see that we need to turn to one of the more influential papers published in ecology, by a natural historian named Stephen A. Forbes.
The Legacy of the Little Mentioned Stephen A. Forbes
Stephen Forbes was a broadly trained naturalist, one of the last in the tradition of Darwin and Huxley, Gray and Agassiz. In 1887, he published a classic paper entitled, "The Lake as a Microcosm", which is generally recognized as one of the first statements of the ecosystem concept. This was a very popular essay, and was reprinted in 1925, and has been continually read by subsequent generations of ecologists. What is interesting is that he grew up during the Civil War period, and his training was primarily in entomology, although he had strong interests in botany. After a period of scientific investigation, he was named as a professor at Illinois State Normal University in 1875, and finally made chair of zoology in 1884. At that time, he was given an honorary doctorate, since he had no college degrees up to that time.
Forbes' contribution was that the lake had two primary characteristics: the concept of a community (organisms interacting with each other, predator-prey, etc.) and second, that the community had evolved to achieve the order seen at the whole lake level. Although the language today is antiquated, it represented the standard literary style for that period. It had strong influences on subsequent ecologists. For example, Forbes used such terms as "fearful slaughter", and a "scramble for food". Forbes also envisioned the lake as both mechanical and organic. It's parts worked together like a machine, but the parts were living organisms. Forbes analyzed stomach contents of bass, and knew what was prey, and what was predator, and that the survival of the bass was directly dependent on its food sources, which were highly varied. In addition, he appreciated the fact that these myriad interactions served to regulate populations within the lake so that the lake appeared in equilibrium. But equilibrium did not mean that all was peaceful, and that populations never increased, or decreased, but rather, that the panoply of species interactions, however chaotic they might have seemed, balanced one another, so that at the level of the lake, the ecosystem, it appeared that nature was in equilibrium.
The choice of the term "community" probably came out of Forbes' thoughts that these organisms interacted much like a community of people, and the term became standard ecological terminology.
So, in conclusion, Forbes anticipated some trends and analogies that would become standard place in future generations of ecologists, namely the interdependence of species on one another, the metaphor of the lake as machine, and the nature of stability and instability as a function of individual species interactions. But Forbes was careful not to view the lake as a superorganism, as a later ecologist would, but rather a system of interacting species that could be modeled as a whole. But the lake was not an organism unto itself. However, as we shall see, there was one ecologists who took the superorganism concept far beyond what Forbes envisioned. His name was Frederick Edward Clements.
Frederick Edward Clements and the SuperOrganismal Concept
Perhaps no single ecologist has had the lasting imprint of F.E. Clements. While his ideas regarding the community as an organism have been discredited this century, his impact on the development of ecology as a scientific discipline and his concentration on the process of succession have endured until this day.
Clements was a skilled botanist, somewhat aloof and diffident, but of keen intellect. He saw a need for ecology to get away from simply describing communities (a lasting residue from the Victorian age and the 19th century model of the naturalist) to investigating them using the scientific method, much like physicists investigated their discipline, or chemists theirs. Clements wanted ecology to be a rigorous, experimental science, and his approach was to try to understand community processes by understanding the physiology of its constituent parts, the plants and animals: "...a rational field physiology."
Much of the inspiration Clements and other budding ecologists had came in no small part from their location in the midwest of the United States. At that time, as the frontiers were closing in, there were still abundant natural communities to study, including forests, lakes, and prairies. Also, new institutions of higher learning were springing up, most notably the University of Chicago, which attracted some of the best and brightest minds in this newly emerging field. Here, the new scientists could form new departments and research groups, essentially starting de novo, and freed from the traditional trappings that constrained more conservative eastern universities. Thus, many of the early advances in ecology, and in particular, ecosystem ecology, first appeared in the midwestern universities and research institutions.
But first a digression. One of the most influential of the early ecologists was the botanist Henry Chandler Cowles. Cowles did his graduate work at the University of Chicago, and then stayed there as a professor the rest of his career. He worked on succesional changes in plant communities on the sand dunes surrounding Lake Michigan.
His research was characterized by careful observation, and speculative theorizing (Hagen pg. 17). He grouped plants into communities, such as perennial herbs, heath, coniferous forest, and deciduous forest, and then, importantly, arranged them into a developmental sequence as he thought occurred as dunes were colonized by plants. His inspiration for studying dunes came from the work of a Danish ecologist who studied dunes in Europe, Eugenius Warming. Both men shared a desire to work with plant communities, and to attribute their existence and persistence to the physiological characteristics of the plants contained therein. Cowles added one aspect that was perhaps underemphasized by Warming, and that was the strong influence of the underlying geology, a love of Cowles since his school days. He showed that the soil type could be influenced by the bedrock, and that the soil type often altered the type of community one might expect in an area. In addition, the research tradition of geology offered a scenario by which Cowles could conduct his investigations. As he wrote:
"Such a study is to structural botany what dynamical geology is to structural geology. Just as modern geologists interpret the structure of the rocks by seeking to find how and under what conditions similar rocks are formed today, so ecologists seek to study those plant structures which are changing at the present time, and thus to throw light on the origin of plant structures themselves."
We should make it clear that although Cowles used organic analogies throughout his writings, as did most other ecologists, he did not believe that the community was in and of itself, a living superorganism. One of the important contributions Cowles made to ecology was to show how important competition could be in structuring plant communities. He showed, for example, that pine forests were replaced by oak forests not because pines were poorly adapted to the underlying soils, but simply because the oaks were superior competitors on that site. These studies of Cowles became classic examples of the successional process, and had a strong influence on future ecologists also. Some fifty years later, Jerry Olson did contemporary studies on those same dunes, and his research won awards. Eugene Odum, the dean of 20th century ecologists, has said that Cowles' research had the same relative impact on ecology as did Mendel's research in genetics. Odum considered the study of succession central to understanding ecosystems. But Cowles never was able to outgrow his natural history upbringing, and aside from his successional studies, and some speculative theorizing, he never achieved a synthesis beyond the community level. That was left for subsequent generations. Now, back to F.E. Clements.
The Philosophy of Clements
Clements spent most of his active career life outside of traditional academia. After obtaining a post at the University of Nebraska (where he studied under Bessey, the great botanist), he was offered a position at the new established Carnegie Institute of Washington, where he spent the rest of his career. His diffident personality did not endear him to either his colleagues at Nebraska, or to his students, in contrast to that of Cowles, who was a much loved teacher. Because of this, Cowles left a long legacy of students who eventually became ecologists, whereas Clements did not. Clements' influence came from his keen intellect, and his writings, which were voluminous, and less so from his legacy as a great teacher.
Clements extended and developed the concept of the community as an organism, using explicit organic analogies. He often referred to the community as a "complex organism" and succession was its life cycle (Hagen pg. 22). Clements, according to Hagen, did not mean to imply that communities were similar to higher organisms literally, but perhaps, more closely resembled the life cycles of protists and other smaller organisms. But Clements was not naive, and never intended that a community was the exact same thing as a living organism. But he grounded his analogy in physiology, and viewed the study of communities as essentially the study of physiological processes. His call to ecologists was to get out of the lab, and into the field.
However, Clements was also a neo-Lamarckian, who thought that environmental cues to plants could be passed onto to future generations. This may sound heretical, but in fact, at the turn of the century, just when Mendel's laws were being rediscovered, it was not all that unusual. Of course those ideas were wrong, but it influenced his writings and persisted well past the point where most ecologists and biologists had dismissed Lamarckism in favor of Darwin's theory of natural selection. When he died in 1945, his Lamarckian ideas were totally out of favor in the scientific community.
His lasting reputation was made with his studies of succession, beginning in his early book Research Methods in Ecology (1905), and culminating in his most important contribution, Plant Succession (1916). It immediately became a focus of attention in the ecological community, and even today scientists refer to it for introspect and historical purposes. Clements philosophy was simple, according to Hagen (pg. 25):
"...plants invaded an area, they competed, they reacted to the physical environment, and they modified it. Each process could be understood in terms of simple stimulus-response mechanisms."
"Competition is purely a physical process. With few exceptions...an actual struggle between competing plants never occurs. Competition arises from the reaction of one plant upon the physical factors about it and the effect of these modified factors upon its competitors."
For example, water absorbed by one plant is not available to another plant, and light absorbed by a taller plant prevents a lower one from getting it.
Clements built on these ideas to explain the successional process as one in which the results of competition change the species composition of an area, which then compete, and further change the community, until a final, climax stage is reached, in which those plants still remaining co-exist indefinitely in the absence of disturbance. "...a climax", wrote Clements "is permanent because of its entire harmony with a stable habitat. It will persist just as long as the climate remains unchanged, always providing that migration does not bring in a new dominant from another region."
The idea of stable climaxes have proven the most controversial of all of Clements' statements. While later ecologists criticized the idea of a monoclimax in any one region, according to Hagen (pg. 27) they also failed to appreciate that Clements himself had some reservations about the stability of climax vegetation. He wrote "The most stable association is never in complete equilibrium." He knew, from his extensive field work, that communities changed with time, and that climaxes were not static entities, but shifted depending on the climate and other exogenous factors.
What upset ecologists about Clements' views was his insistence that communities were co-evolved complexes, that given enough time, would re-appear in the landscape, as long as the climate was the same. His critics viewed the community not as a co-evolved collection of adapted species, but a random mixture of species which co-existed because of their similar physiological and ecological adaptations. The most foremost proponent of this individualistic concept was Henry A. Gleason, a botanist affiliated with the New York Botanical Garden.
Attacks on the Clementsian Doctrine
Gleason vehemently disagreed that communities represented co-evolved sets of species, and published several articles against the concept. He based his ideas on three premises: environmental factors vary in space and time, each plant species has its own tolerance of these factors, and plants tend to disperse their seeds randomly. Together, these all added up to the idea that communities were random collections of species that were able to tolerate each other and the environment, and thus, co-exist. This meant that communities had no set boundaries, or that communities changed en masse as one moved along an environmental gradient. Gleason even wrote that communities were "...merely abstractions of the ecologist's mind."
It is interesting though, that in his two main articles, Gleason never directly mentioned Clements' work directly. And Clements, who held Gleason in low regard, never rebutted the attacks. But Gleason's ideas never took hold until after WWII, in part because other ecologists did not know much about Gleason, and were reluctant to side with an unknown, and partly because he was not at a university setting, which might have hurt his prestige with other academics. More importantly, Gleason's papers were theoretical constructs, and he never personally collected data to back up his claims. That rested with later ecologists, most notably John T. Curtis and Robert H. Whittaker, whose extensive studies of environmental gradients, labeled gradient analyses by the Curtis school at Wisconsin, finally confirmed much of what Gleason had postulated.
But there were valid criticisms of Gleason's reasoning. For example, as Hagen (pg. 30) points out, the idea "...that communities are not organisms because they lack distinct boundaries is an obvious non sequitur. Humans and some other animals may have rather definite external boundaries, but many other types of organisms do not; this distinction was pointed out by organismal thinkers both before and after Gleason's day." Gleason's heavy dependence on randomness upset ecologists, because it seemed to preclude any possibility of general laws for succession, the question of which was still much in debate.
The studies by Curtis and Whittaker clearly demonstrated that the transition between communities occurs without sharp lines of demarcation, clearly vindicating some of the ideas of Gleason. Whittaker's study of the community transitions in the Smokies (1956) is a classic, and still used by ecologists today, including me! Whittaker suggested that climaxes came in all sorts of types, and proposed the concept of the shifting climax, wherein late successional vegetation moves around in the landscape depending on the vagaries of the climate, soil, and weather. A true climax is a mosaic of vegetation stages.
The Legacy of Clements
Although many of Clements ideas did not survive him, such as his Lamarckian views, his insistence that succession was always linear and progressive (Watt, in 1947, wrote a classic paper on cyclic succession, wherein the vegetation goes from state A->B->C->D and then back again to state A. This contradicted Clements' view that once a climax was reached, it persisted). And Clements' mechanistic ideas for how plants succeeded each other was viewed by physiologists as hopelessly simplistic, and his thoughts on climaxes have been superceded by more sophisticated ones.
But the enduring legacy of Clements is that he caused to ecologists to think about the "big picture", to integrate both abiotic and biotic factors in their analysis of community dynamics, and to begin to devise experimental methods to deal with community problems. His emphasis on process studies, rather than 19th century descriptive studies was perhaps his greatest contribution to ecology.
Clements, Frederick E. 1905. Research Methods in Ecology. University Printing Co., Lincoln.
Clements, Frederick E. 1916. Plant Succession: An Analysis of the Development of Vegetation. Carnegie Institution of Washington, Washington, DC.
Cowles, Henry C. 1899. The ecological relations of the vegetation on the sand dunes of Lake Michigan. Botanical Gazette 27:95-117. See also pgs. 167-202, 281-308, 361-391.
Forbes, Stephen A. 1925. The lake as a microcosm, Bulletin of the Illinois Natural History Survey 15:537-550 (originally published in 1887 in the Bull. Peoria Scientific Association).
Gleason, Henry A. 1926. The individualistic concept of the plant association. Bulletin of the Torrey Botanical Club 53:7-26. Also see revised article with same title in American Midland Naturalist 21:92-110.
Olson, Jerry S. 1958. Rates of succession and soil changes on southern Lake Michigan sand dunes. Botanical Gazette 119:125-170. This paper won the prestigious Mercer Award for young ecologists from the Ecological Society of America.
Spencer, Herbert. 1860. The Social Organism, in his The Man Versus the State, edited by Donald MacRae (The Westminster Review, January 1860), Penguin Books, 1969.