Osmotrophy in modular Ediacara organisms

Abstract

The Ediacara biota include macroscopic, morphologically complex soft-bodied organisms that appear globally in the late Ediacaran Period (575-542 Ma). The physiology, feeding strategies, and functional morphology of the modular Ediacara organisms (rangeomorphs and erniettomorphs) remain debated but are critical for understanding their ecology and phylogeny. Their modular construction triggered numerous hypotheses concerning their likely feeding strategies, ranging from micro-to-macrophagus feeding to photoautotrophy to osmotrophy. Macrophagus feeding in rangeomorphs and erniettomorphs is inconsistent with their lack of oral openings, and photoautotrophy in rangeomorphs is contradicted by their habitats below the photic zone. Here, we combine theoretical models and empirical data to evaluate the feasibility of osmotrophy, which requires high surface area to volume (SA/V) ratios, as a primary feeding strategy of rangeomorphs and erniettomorphs. Although exclusively osmotrophic feeding in modern ecosystems is restricted to microscopic bacteria, this study suggests that (i) fractal branching of rangeomorph modules resulted in SA/V ratios comparable to those observed in modern osmotrophic bacteria, and (ii) rangeomorphs, and particularly erniettomorphs, could have achieved osmotrophic SA/V ratios similar to bacteria, provided their bodies included metabolically inert material. Thus, specific morphological adaptations observed in rangeomorphs and erniettomorphs may have represented strategies for overcoming physiological constraints that typically make osmotrophy prohibitive for macroscopic life forms. These results support the viability of osmotrophic feeding in rangeomorphs and erniettomorphs, help explain their taphonomic peculiarities, and point to the possible importance of earliest macroorganisms for cycling dissolved organic carbon that may have been present in abundance during Ediacaran times.erniettomorphs ͉ rangeomorphs ͉ Fractofusus ͉ Pteridinium

Ediacaran developmental biology

“…Specimens of Pteridinium can taper at one or both ends, with the tapering tip previously inferred to be the growth tip (Grazhdankin & Seilacher, 2002; Laflamme, Xiao, & Kowalewski, 2009). Pteridinium has thus been variously considered as both unipolar (Grazhdankin & Seilacher, 2002) and bipolar (Laflamme et al ., 2009), although the lack of a tapering tip in some specimens may reflect a taphonomic bias (Seilacher, 1989).…”

“…Pteridinium has thus been variously considered as both unipolar (Grazhdankin & Seilacher, 2002) and bipolar (Laflamme et al ., 2009), although the lack of a tapering tip in some specimens may reflect a taphonomic bias (Seilacher, 1989). The distal‐most unit can be positioned on either side of the central seam, suggesting that Pteridinium added units sequentially across its different vanes (Tojo et al ., 2007; although see Laflamme et al ., 2009).…”

“…Pteridinium has thus been variously considered as both unipolar (Grazhdankin & Seilacher, 2002) and bipolar (Laflamme et al ., 2009), although the lack of a tapering tip in some specimens may reflect a taphonomic bias (Seilacher, 1989). The distal‐most unit can be positioned on either side of the central seam, suggesting that Pteridinium added units sequentially across its different vanes (Tojo et al ., 2007; although see Laflamme et al ., 2009). Pteridinium has previously been considered to grow mainly by the ‘insertion’ of new units over time (Laflamme et al ., 2009), but it appears that one morph also grew by the observable inflation of pre‐existing units (Grazhdankin & Seilacher, 2002).…”

“…The distal‐most unit can be positioned on either side of the central seam, suggesting that Pteridinium added units sequentially across its different vanes (Tojo et al ., 2007; although see Laflamme et al ., 2009). Pteridinium has previously been considered to grow mainly by the ‘insertion’ of new units over time (Laflamme et al ., 2009), but it appears that one morph also grew by the observable inflation of pre‐existing units (Grazhdankin & Seilacher, 2002). Specimens that are ∼6 cm long have been inferred to be immature (Grazhdankin & Seilacher, 2002), but there are no documented specimens of comparable size to those of the smallest rangeomorphs and dickinsoniomorphs (i.e.…”

Was the Ediacaran–Cambrian radiation a unique evolutionary event?

“…Grazing mesoplankton and filter-feeding metazoans created the modern biological pump and helped ventilate the water column (Butterfield 2009). By the second half of the Ediacaran, environments were dominated by microbial substrates and most Ediacara macrofossils were likely osmotrophic, feeding on dissolved organic carbon (DOC) (Laflamme et al 2009;Sperling et al 2011), a very limited trophic resource today. Macroscopic grazing habits appeared with Kimberella about 555 Ma (Fedonkin et al 2007).…”