From the Cover: 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.

Fig. 1.

Modular Ediacara fossils. (A) Three incomplete specimens of the erniettomorph fossil Pteridinium composed of tubular modular units. (B) Pteridinium with nine modular units (right side of fossil). (C) Erniettomorph Ernietta with module infilling. (D) Magnified section of the specimen in the boxed section in C, with arrows highlighting sediment infill. (E) Rangeomorph fossil Rangea with fractal modules (bracket on the right). (F) Rangea with three primary fractal modules (large modules on the left) and three smaller subsidiary modules tucked in between the larger modules. (G) Rangeomorph Fractofusus with 16 fractal modules on either side of the longitudinal midline. Bracket displaying one module. G is provided by G.M. Narbonne. (Scale bar: 1 cm.)

Fig. 2.

Modeling parameters of erniettomorphs and rangeomorphs. (A) Width (a), length (b), and hollowness (c) of an erniettomorph module. (B) Bipolar addition of erniettomorph module triplets during growth (t = 0, 1, 2…). (C) Overlap (1 = full, 0 = none) between erniettomorph modules was simulated to compare tightly packed vs. loosely overlapping modules. (D) Fractal subdivision of a rangeomorph module.

Fig. 3.

Growth variations in Pteridinium and Fractofusus. (A) Plot of the number of modules and the maximum module width vs. the overall length of each of the 11 complete Pteridinium specimens from Namibia (6). The plot shows that Pteridinium grew mostly by module addition, not module inflation. (B) Plot of the number of modules and the maximum module length (equal to half of specimen width) vs. the overall length of each of the 66 complete Fractofusus specimens from Newfoundland (18), showing that growth was through module inflation, with minor contribution from module addition during early growth. Spearman Rank Correlation values (r) for Pteridinium: length vs. module width: r = 0.66 (P = 0.03); length vs. number of modules: r = 0.92 (P < 0.0001); for Fractofusus: length vs. module width: r = 0.91 (P < 0.0001); length vs. number of modules: r = 0.49 (P < 0.0001).

Fig. 4.

Effect of hollowness in Pteridinium (A) and fractal branching in Fractofusus (B) on their SA/V ratios. (A) Estimated SA/V ratios of a Pteridinium specimen consisting of 100 triplets of the smallest (length b = 37 mm, width a = 2.4 mm; black circle), average (b = 55 mm, a = 3.2 mm; dark gray circle), and largest (b = 82 mm, a = 3.6 mm; light gray circle) modules that have full overlap. Modular sizes based on measurements of Pteridinium specimens from Namibia (6). Colored squares represent the effect of hollowness (purple: thickness of metabolically active material, c = 1 mm; yellow, c = 0.5 mm; blue, c = 0.1 mm; and green, c = 0.01 mm). Filled squares represent instances where modules are terminally closed, whereas open squares represent distally open modules in which the internal surface area of modules could also be used for diffusion. All square-symbol models used 100 module triplets with an average module size and full overlap. (B) Increase in Fractofusus SA/V ratios with incremental fractal branching (blue diamonds, fractalless modules; red squares, one order of fractal branching; green triangles, two orders of fractal branching; purple circles, three orders of fractal branching; and blue stars, four orders of fractal branching). Modular sizes based on measurements of Fractofusus specimens from Newfoundland (18). Diamonds in A and B represent SA/V ratios of modern megabacteria. Note Thiomargarita full vs. thin distinguishes between gross SA/V ratio (the entire cell was biologically active) vs. effective SA/V ratios (active organic matter was restricted to a 0.5-μm peripheral layer). Only gross SA/V ratios are presented for all other megabacteria.