The rangeomorph Pectinifrons abyssalis: Hydrodynamic function at the dawn of animal life

Abstract

Rangeomorphs are among the oldest putative eumetazoans known from the fossil record. Establishing how they fed is thus key to understanding the structure and function of the earliest animal ecosystems. Here, we use computational fluid dynamics to test hypothesized feeding modes for the fence-like rangeomorph Pectinifrons abyssalis, comparing this to the morphologically similar extant carnivorous sponge Chondrocladia lyra. Our results reveal complex patterns of flow around P. abyssalis unlike those previously reconstructed for any other Ediacaran taxon. Comparisons with C. lyra reveal substantial differences between the two organisms, suggesting they converged on a similar fence-like morphology for different functions. We argue that the flow patterns recovered for P. abyssalis do not support either a suspension feeding or osmotrophic feeding habit. Instead, our results indicate that rangeomorph fronds may represent organs adapted for gas exchange. If correct, this interpretation could require a dramatic reinterpretation of the oldest macroscopic animals.

Keywords: Evolutionary biology; Paleobiology; Zoology.

Graphical abstract

Figure 1

Pectinifrons abyssalis from Mistaken Point, Newfoundland, Canada (A–C) Photographs of steep ‘U’-shaped (A), ‘S’-shaped (B), and gentle ‘U’-shaped (C) morphotypes of Pectinifrons. Scale bars: 5 cm. (D) Schematic diagrams of Pectinifrons morphotypes.

Figure 2

Digital models and computational domain (A–D) Digital models of steep ‘U’-shaped (A), ‘S’-shaped (B), and gentle ‘U’-shaped (C) morphotypes of Pectinifrons and three-vaned C. lyra (D). (E and F) Computational domain used in CFD simulations. (G) Horizontal cross-section (z = 2 cm) through mesh used in CFD simulations for refinement area shown in (F). Scale bars: 10 cm. See also Figure S1.

Figure 3

Two-dimensional plots (horizontal and vertical cross-sections) of velocity magnitude (U) with flow vectors (size of gray arrows proportional to natural logarithm of velocity magnitude) at an inlet velocity of 0.1 m/s for three Pectinifrons models Different Pectinifrons morphotypes (i.e., ‘U’- and ‘S’-shaped) are arranged in rows, while models in different orientations to current (i.e., 0°, 90°, and 180°) are arranged in columns. Within each panel, the uppermost plot shows a horizontal cross-section (z = 2 cm), while the bottom two panels show vertical cross-sections (gentle ‘U’-shaped model at 0° and 180°, upper plots y = 23 cm and lower plots y = 0 cm; gentle ‘U’-shaped model at 90°, upper plot y = 7 cm and lower plot y = 0 cm; steep ‘U’-shaped model at 0° and 180°, upper plots y = 18 cm and lower plots y = 0 cm; steep ‘U’-shaped model at 90°, upper plot y = 7 cm and lower plot y = 0 cm; ‘S’-shaped model at 0°, upper plot y = 22 and lower plot y = 0 cm; ‘S’-shaped model at 90°, upper plot y = 5 cm and lower plot y = 0 cm). Direction of ambient flow in each panel is from left to right. Scale bar: 10 cm. See also Figures S3 and S4.

Figure 4

Three-dimensional isosurface plots of negative values of velocity component u (streamwise velocity) at an inlet velocity of 0.1 m/s for three Pectinifrons models Different Pectinifrons morphotypes (i.e., ‘U’- and ‘S’-shaped) are arranged in rows, while models in different orientations to current (i.e., 0°, 90°, and 180°) are arranged in columns. Results for our ‘S’-shaped model at 0° and 180° are identical, and so the latter is not shown. Direction of ambient flow in each panel is from top left to bottom right. Scale bar: 10 cm. See also Figures S5 and S6.

Figure 5

Two-dimensional plots (vertical cross-sections) of turbulent kinetic energy magnitude (k) at an inlet velocity of 0.1 m/s for three Pectinifrons models Different Pectinifrons morphotypes (i.e., ‘U’- and ‘S’-shaped) are arranged in rows, while models in different orientations to current (i.e., 0°, 90°, and 180°) are arranged in columns. Within each panel, the uppermost plot shows a vertical cross-section toward the margin of the model (gentle ‘U’-shaped model at 0° and 180°, y = 23 cm; gentle ‘U’-shaped model at 90°, y = 7 cm; steep ‘U’-shaped model at 0° and 180°, y = 18 cm; steep ‘U’-shaped model at 90°, y = 7 cm; ‘S’-shaped model at 0°, y = 22; ‘S’-shaped at 90°, y = 5 cm), while the lower plot shows a vertical cross-section at the approximate center of the model (y = 0 cm). Direction of ambient flow in each panel is from left to right. Scale bar: 10 cm. See also Figures S7 and S8.

Figure 6

Three-dimensional isosurface plots of turbulent kinetic energy magnitude (k) at an inlet velocity of 0.1 m/s for three Pectinifrons models Different Pectinifrons morphotypes (i.e., ‘U’- and ‘S’-shaped) are arranged in rows, while models in different orientations to current (i.e., 0°, 90°, and 180°) are arranged in columns. Results for our ‘S’-shaped model at 0° and 180° are identical, and so the latter is not shown. Direction of ambient flow in each panel is from top left to bottom right. Scale bar: 10 cm. See also Figures S9 and S10.

Figure 7

Two-dimensional plots (horizontal and vertical cross-sections) of velocity magnitude (U) with flow vectors (size of gray arrows proportional to natural logarithm of velocity magnitude) at an inlet velocity of 0.1 m/s for two C. lyra models C. lyra morphotypes (i.e., three- and two-vanes) are arranged in rows, while models in different orientations to current (i.e., 0°, 90° and 270°) are arranged in columns. Within each panel, the uppermost plot shows a horizontal cross-section (z = 5 cm), while the bottom two panels show vertical cross-sections (three vaned model at 0°, upper plot y = 28 cm and lower plot y = 0 cm; three vaned model at 90° and 270°, upper plots y = 24 cm and lower plots y = 0 cm; two vaned model at 0°, upper plot y = 28 cm and lower plot y = 0 cm; two vaned model at 90°, y = 0 cm). Results for our two-vaned model at 0° and 180° are identical, and so the latter is not shown. Direction of ambient flow in each panel is from left to right. Scale bar: 10 cm. See also Figures S14 and S15.

Figure 8

Three-dimensional isosurface plots of negative values of velocity component u (streamwise velocity) at an inlet velocity of 0.1 m/s for two C. lyra models C. lyra morphotypes (i.e., three- and two-vanes) are arranged in rows, while models in different orientations to current (i.e., 0°, 90°, and 180°) are arranged in columns. Results for our two-vaned model at 0° and 180° are identical, and so the latter is not shown. Direction of ambient flow in each panel is from top left to bottom right. Scale bar: 10 cm. See also Figures S16 and S17.