Gill function in an early arthropod and the widespread adoption of the countercurrent exchange mechanism

Abstract

Rising but fluctuating oxygen levels in the Early Palaeozoic provide an environmental context for the radiation of early metazoans, but little is known about how mechanistically early animals satisfied their oxygen requirements. Here we propose that the countercurrent gaseous exchange, a highly efficient respiratory mechanism, was effective in the gills of the Late Ordovician trilobite Triarthrus eatoni. In order to test this, we use computational fluid dynamics to simulate water flow around its gills and show that water velocity decreased distinctly in front of and between the swollen ends, which first encountered the oxygen-charged water, and slowed continuously at the mid-central region, forming a buffer zone with a slight increase of the water volume. In T. eatoni respiratory surface area was maximized by extending filament height and gill shaft length. In comparison with the oxygen capacity of modern fish and crustaceans, a relatively low weight specific area in T. eatoni may indicate its low oxygen uptake, possibly related to a less active life mode. Exceptionally preserved respiratory structures in the Cambrian deuterostome Haikouella are also consistent with a model of countercurrent gaseous exchange, exemplifying the wide adoption of this strategy among early animals.

Keywords: Gill; computational fluid dynamics; efficient mechanisms; metazoans; respiration.

Figure 1.

Interaction of haemolymph flow and water current. (a) Cross-section of the filament of T. eatoni, YPM 204. (b) Reconstructed cross-section showing haemolymph flow. (c) Upstroke of gill branch creates downward-flowing water current, opposite to upward-directed haemolymph flow. (d) Reverse stroke of gill branch creates upward-flowing water current, same direction as upward-directed haemolymph flow. (e) Anticlockwise rotation of gill branch creates posteriorly downward-flowing water current, reverse of upward-directed haemolymph flow. (f) Reverse stroke of gill branch creates upward-flowing water current, same direction with upward-directed haemolymph flow. (g) Any water current flowing downward is always paired with the countercurrent haemolymph flow. (h) A countercurrent exchange model shows how the opposite flow exchanges oxygen with gradient difference. Pink dash line with arrow represents the possible routes for haemocyanin from bottom to top side. Black dashed line with arrow represents the water current and its direction. The light blue background represents the water medium. Arabic numbers in (e) represent paired countercurrent flow. ac, afferent channel; av, afferent vessel; ec, efferent channel; ev, efferent vessel; db, down backward rotation; ds, downstroke; hem flow, haemolymph flow; ncr, narrow central region; uf, up forward rotation; us, upstroke; wat cur, water current; rs, reverse stroke. Scale bar, 0.05 mm (a).

Figure 2.

Detailed description of gills. (a) Well-preserved gill branches of trilobite T. eatoni, GLAHM 163103. (b) Reconstructed partial gill branch of T. eatoni. The area marked with a black box is the target of computational fluid dynamics (CFD) analysis. Cross-section of the gill filaments shows dumbbell-shaped outline and interspace among filaments. Water currents (marked with black arrows) flow through the interspace between filaments. (c) Three types of gill models (10 times actual size) of T. eatoni examined in this study: reduced cylinder, dumbbell shape and inflated cylinder. (d) Simplified gill models: trilobite, fish and crab showing critical features. (e) Simplified cross-section of respiratory filament of crab gills showing the diffusion distance, a possible analogue applicable to trilobite gills. an, anterior; cu, cuticle; d, interfilament or interlamellar distance; dor, dorsal; dd, diffusion distance (or barrier); ep, epithelium; fl, filament; gr, gill raphe; h, height; l, length; hv, haemolymph vessel; in, innerward; la, lamella; ou, outward; pc, pillar cell; sh, shaft; ven, ventral; w, width.

Figure 3.

CFD simulations of water current flowing through three gill filament morphologies (shown as cross-sections). (a) Three different flow velocities simulated for dumbbell shape model. (b) Comparison of three types of models under the same flow velocity. Water flows from left to right. The velocities on the bottom represent the inlet flow velocity. The colour range of the scale bars starts from the 0 m/s to the maximum which is same as the inlet flow velocity.

Figure 4.

Details of flow velocity among filaments. (a) Reduced cylinder model showing uniformly high-speed flows among filaments. (b) Dumbbell model showing a buffer zone (marked with a yellow star) centrally that expands water laterally. (c) Inflated cylinder model showing uniformly low-speed flow among filaments. Water flows from left to right in this diagram and the velocity of the incoming flow is 0.05 m s⁻¹ (inlet flow). The colour range of the velocity map in this figure is, however, visually restricted between 0 and 0.001 m s⁻¹, which is designed for displaying the micropatterns of flow paths.

Figure 5.

Comparison of oxygen capacity among fish and arthropods. Original data are available in electronic supplementary material, file. VO₂, oxygen volume.

Figure 6.

Gaseous exchange in chordate Haikouella jianshanensis. (a) Well-preserved gills of H. jianshanesis bearing a backward curved central supporting structure which is attached with many filaments that have a wide base and pointed end, specimen 146 [24]. (b) Gills of H. jianshanensis, specimen 088 [24]. (c) Reconstruction of gill cross-section of H. jianshanesis showing afferent and efferent vessels (based on [24], fig. 2g). Black dashed lines with arrows represent possible posterior water current flow. Purple dotted arrow is the oxygen charging path of individual haemocyanin, replacing lower concentration of oxygen with high concentration of oxygen. Suggested water current over the gill filaments from outer surface to inner surface, which permits countercurrent oxygen exchange with haemolymph flowing inside gill filaments. ac, afferent channel; ec, efferent channel; gs, gill supporting structure; gf, gill filament. Scale bars, 5 mm (a) and 2 mm (b).