Atmosphere, ecology and evolution: what drove the Miocene expansion of C4grasslands?

Abstract

1 Grasses using the C₄ photosynthetic pathway dominate today's savanna ecosystems and account for ~20% of terrestrial carbon fixation. However, this dominant status was reached only recently, during a period of C₄ grassland expansion in the Late Miocene and Early Pliocene (4–8 Myr ago). Declining atmospheric CO₂ has long been considered the key driver of this event, but new geological evidence casts doubt on the idea, forcing a reconsideration of the environmental cues for C₄ plant success. 2 Here, I evaluate the current hypotheses and debate in this field, beginning with a discussion of the role of CO₂ in the evolutionary origins, rather than expansion, of C₄ grasses. Atmospheric CO₂ starvation is a plausible selection agent for the C₄ pathway, but a time gap of around 10 Myr remains between major decreases in CO₂ during the Oligocene, and the earliest current evidence of C₄ plants. 3 An emerging ecological perspective explains the Miocene expansion of C₄ grasslands via changes in climatic seasonality and the occurrence of fire. However, the climatic drivers of this event are debated and may vary among geographical regions. 4 Uncertainty in these areas could be reduced significantly by new directions in ecological research, especially the discovery that grass species richness along rainfall gradients shows contrasting patterns in different C₄ clades. By re-evaluating a published data set, I show that increasing seasonality of rainfall is linked to changes in the relative abundance of the major C₄ grass clades Paniceae and Andropogoneae. I propose that the explicit inclusion of these ecological patterns would significantly strengthen climate change hypotheses of Miocene C₄ grassland expansion. Critically, they allow a new series of testable predictions to be made about the fossil record. 5 Synthesis. This paper offers a novel framework for integrating modern ecological patterns into theories about the geological history of C₄ plants.