History of the Concept of Coevolution of Biosphere and Climate

Vladimir Vernadsky (1863-1945) should be regarded as the father of biogeochemistry, having coined the word in 1926 in his book on the biosphere. For Vernadsky, the central concept of biogeochemistry, the intersection of the biological, geological, and chemical, is the cycling of elements through the biosphere. Vernadsky had a profound influence on the subsequent development of biogeochemistry in the West since his son George was a professor at Yale, and a friend of G. E. Hutchinson, an influential force in the development of ecology, biogeo-chemistry, and limnology.

Ecologists have long recognized the coevolution of life and its environment, following Darwin's theory, but the 'environment' with rare exceptions refers to the immediate local influences on the organism. This insight has now been developed in depth with the theory of niche construction, which follows up Richard Lewontin's concept of organism/environment coevolution.

A much more radical conception of coevolution was put forward by James Lovelock, an atmospheric chemist, soon joined by Lynn Margulis (the biologist best known for her theory of endosymbiogenesis), namely the Gaia hypothesis. Lovelock argued that the classical view of coevolution of climate and life neither captures the richness of interactive processes and feedbacks, nor recognizes that planetary biota actively determines its planetary environment. But Lovelock goes even further, asserting that in some sense the Earth (surface) is living, with its own physiology, a 'geophysiology' of a superorganism,with even homeostasis, a general characteristic of metabolism. Biotic regulation of its global external environment leading to, for example, stable climate is for Lovelock homeostasis on a planetary scale.

The Earth as a 'superorganism' resonates with the conception of Hutton, the eighteenth-century Scottish doctor and farmer, generally regarded as the founder of modern geology.

Lovelock argued that the Earth's habitability for the last 3 billion years (now accepted for at least 3.5 billion years based on fossil evidence) was a result of continuous biotic interaction with the other components of the biosphere: the atmosphere, ocean, and soil/upper crust. The requirements of habitability include favorable temperatures, ocean salinity, and, at least for the last 2 billion years, atmospheric oxygen at aerobic levels. In Lovelock and Margulis' early papers, we find a formulation of Gaia as a homeostatic system.

From the fossil record it can be deduced that stable optimal conditions for the biosphere have prevailed for thousands of millions of years. We believe that these properties of the terrestrial atmosphere are best interpreted as evidence of homeostasis on a planetary scale maintained by life on the surface. (Lovelock and Margulis, 1974)

However, the concept of optimality is highly problematic: optimal for the persistence of planetary biota, but which components? Is optimality to be measured in the number of species? Did the anaerobic prokaryotes of the Archean have the foresight to optimize atmospheric conditions for their successors, the aerobes?

As a result of sustained challenges to 'homeostatis' Gaia, Lovelock reformulated his original concept as 'geo-physiological' Gaia, ''a theory that views the evolution of the biota and of their material environment as a single, tightly coupled process, with the self-regulation of climate and chemistry as an emergent property'' (Lovelock, 1989). Thus, the biosphere is now seen as an evolving system with negative feedback such as climatic stabilization.

However, biological regulation may well be limited to restricted 'phase space' - the matrix of physicochemical variables - in biospheric evolution, affecting some conditions but not others (e.g., ocean pH but not salinity), without constituting a global homeostatic system. Another possibility is that for global or regional ecosystems, homeostasis alternates with periods of drift for a given regulated parameter in phase space. This mode has been called 'intermittent Gaia'. Alternatively, homeo-static regulation in some habitats may have persisted since the origin of life. Could this be the case for the 'deep hot biosphere' of the subsurface?

In 'progressive' Gaia, the biota mediates, but both the biota and biosphere coevolve, with no real optimization for the biota at any time. The Gaian research program has proceeded vigorously in its search for self-regulation of other global effects of biotic/biospheric evolution besides the variation of atmospheric oxygen levels, for example, surface temperature, atmospheric composition, as well as for self-regulatory mechanisms operating at smaller scales in the biosphere's subsystems.

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