Ecosystem Succession and Nutrient Retention: Vitousek and Reiners' Hypothesis

Abstract

What mechanisms mediate the flow of energy and cycling of nutrients during ecological succession? Are they linked in time and across space? In 1969, Eugene P. Odum proposed a series of hypotheses that caused the ecological community to think critically about patterns and processes (sensu Watt 1947) during ecological succession and how they might be linked in a causal manner. Odum's perspective on the process of succession, or "the strategy of ecosystem development" as he termed it, was undoubtedly shaped by the intellectual influence of his mentor, Victor Shelford, as well as Shelford's contemporaries such as Fredrick Clements. They shared the idea that ecological communities possessed emergent properties, wherein the whole is greater than the sum of its parts (sensu Phillips 1934). Inasmuch, the 24 hypotheses Odum (1969) articulated were an amalgam of holism and reductionism that created his rationale for the way energy flows and nutrients cycle within ecosystems. It is within this context that Peter Vitousek and Bill Reiners derived ideas that are fundamental to our understanding of energy flow and nutrient cycling in terrestrial ecosystems, ideas that have profoundly shaped my thinking as an ecologist. In his classic paper, Odum (1969) eloquently drew parallels between successional patterns of biomass accumulation in laboratory microcosms and forests, and, moreover, explained how biomass accumulation ceased late in succession because respiration consumed the products of photosynthesis; patterns and processes that he proposed were shared among all ecosystems. He argued further that the "conservation" of growth-limiting plant nutrients should be low in simple, species-poor, early-successional ecosystems, whereas nutrient conservation should be greatest in late-successional ecosystems due to the complexity of biotic interactions among a diverse set of organisms. In retrospect, Odum's rationale regarding the emergence of nutrient conservation from the complexity of late successional ecosystems was probably shaped by a holistic perspective likely derived from his intellectual upbringing, whereas his ideas regarding biomass accumulation were based on physiological observations (e.g., microcosms) and insightful extrapolation (e.g., forests). Odum's attempt to derive pattern from process, or vice versa, fueled the critical thinking of many ecologists, and over the following decades, set in motion events that have generated great insight into ecosystem-level processes. I believe one of the most important was the Nutrient Retention Hypothesis proposed by Peter Vitousek and Bill Reiners. Vitousek and Reiners (1975) revealed a critical disconnect in Odum's rationale for patterns of biomass accumulation and nutrient conservation during secondary succession; Odum failed to realize they were linked, wherein one drove the other. Vitousek and Reiners (1975) argued that, if biomass accumulation in an ecosystem ceased late in secondary succession, then, in contrast to Odum's prediction, nutrient conservation should be low, because the net incorporation of growth-limiting nutrients into living plant biomass also must cease (Fig. 1). This led to the prediction that nutrient retention, or "conservation" as Odum had termed it, should be greatest early in succession when ecosystems are accumulating biomass (i.e., net ecosystem productivity is greater than zero; Fig. 1).