The impact of marine nutrient abundance on early eukaryotic ecosystems

Abstract

The rise of eukaryotes to ecological prominence represents one of the most dramatic shifts in the history of Earth's biosphere. However, there is an enigmatic temporal lag between the emergence of eukaryotic organisms in the fossil record and their much later ecological expansion. In parallel, there is evidence for a secular increase in the availability of the key macronutrient phosphorus (P) in Earth's oceans. Here, we use an Earth system model equipped with a size‐structured marine ecosystem to explore relationships between plankton size, trophic complexity, and the availability of marine nutrients. We find a strong dependence of planktonic ecosystem structure on ocean nutrient abundance, with a larger ocean nutrient inventory leading to greater overall biomass, broader size spectra, and increasing abundance of large Zooplankton. If existing estimates of Proterozoic marine nutrient levels are correct, our results suggest that increases in the ecological impact of eukaryotic algae and trophic complexity in eukaryotic ecosystems were directly linked to restructuring of the global P cycle associated with the protracted rise of surface oxygen levels. Our results thus suggest an indirect but potentially important mechanism by which ocean oxygenation may have acted to shape marine ecological function during late Proterozoic time.

Ediacaran reorganization of the marine phosphorus cycle

“…By 560 Ma, motile macroscopic bilaterians, which would have required more food and oxygen than their sessile ancestors (9), also began to diversify. A direct link between marine P concentration and ecosystem structure and size has also recently been found in an Earth system model (73), consistent with our hypothesis linking these ecosystem changes to increased remineralization of organic phosphorus via sulfate reduction.…”

On the co‐evolution of surface oxygen levels and animals

“…Of note, a recent review of animal ecology across natural gradients in food supply on abyssal plains demonstrated that increased food supply is associated with increases in diversity, animal biomass, sediment mixed‐layer depth, and specialist predator types (Sperling & Stockey, ). These are many of the same ecological changes that are seen across modern oxygen gradients in oxygen minimum zones (OMZs; Rhoads & Morse, ; Sperling, Frieder, et al, ; Sperling, Halverson, et al, ), which are often invoked as prima facie evidence that oxygen changes could have driven the Cambrian radiation (Reinhard et al, accepted).…”

“…However, in recent years there has been an upswing in interest in modeling Proterozoic marine environments and a jump in the complexity of models being utilized. For instance, the intermediate‐complexity Earth system model cGENIE has been utilized by several groups to explore marine redox structure leading up to and during the rise and diversification of metazoans (Reinhard et al, ), and more recently to explore the potential impacts of marine nutrient levels on eukaryotic trophic ecology (Reinhard et al, accepted). As an alternative approach, estimates of marine physical dynamics at various climate states from higher resolution GCMs have been coupled with marine biogeochemical models (Bellefroid et al, ).…”

“…Empirical evidence for low mid‐Proterozoic primary productivity (Crockford et al, ) supports these results. Size‐structured marine ecosystem models embedded within a GCM suggest animals (and even large protists) would have played only a minor role in ecosystems at these reconstructed primary productivity levels (Reinhard et al, accepted). In this light, metazoans simply would not have had the scope to alter biogeochemical cycles in a low‐oxygen Earth system.…”

Coupled Nitrate and Phosphate Availability Facilitated the Expansion of Eukaryotic Life at Circa 1.56 Ga

“…In addition, enhanced phosphorus (P) scavenging in the anoxic, iron rich Mesoproterozoic ocean may have reduced P availability (Derry, 2015; Reinhard et al, 2017; Zegeye et al, 2012). The scarcity of macronutrient elements (N or P, or both) could have limited the rate of primary productivity in the ocean, which, in turn, may have delayed eukaryotic evolution (Anbar & Knoll, 2002; Fennel et al, 2005; Reinhard et al, 2017, 2020).…”