Vertically migrating Isoxys and the early Cambrian biological pump

Abstract

The biological pump is crucial for transporting nutrients fixed by surface-dwelling primary producers to demersal animal communities. Indeed, the establishment of an efficient biological pump was likely a key factor enabling the diversification of animals over 500 Myr ago during the Cambrian explosion. The modern biological pump operates through two main vectors: the passive sinking of aggregates of organic matter, and the active vertical migration of animals. The coevolution of eukaryotes and sinking aggregates is well understood for the Proterozoic and Cambrian; however, little attention has been paid to the establishment of the vertical migration of animals. Here we investigate the morphological variation and hydrodynamic performance of the Cambrian euarthropod Isoxys. We combine elliptical Fourier analysis of carapace shape with computational fluid dynamics simulations to demonstrate that Isoxys species likely occupied a variety of niches in Cambrian oceans, including vertical migrants, providing the first quantitative evidence that some Cambrian animals were adapted for vertical movement in the water column. Vertical migration was one of several early Cambrian metazoan innovations that led to the biological pump taking on a modern-style architecture over 500 Myr ago.

Keywords: Cambrian; Isoxys; biological pump; computational fluid dynamics; pelagic.

Figure 1.

Simplified architecture of the modern biological pump. Arrows trace pathway of carbon (C) and nitrogen (N) and other nutrients. Numbers indicate two main biologically mediated vectors that transport nutrients fixed by phytoplankton from the surface ocean to demersal communities. (1) Aggregation vector of phytoplankton, faecal pellets and other organic matter which sinks passively through the water column. (2) Vertical migration vector driven by active two-way migration by metazoans. (Online version in colour.)

Figure 2.

Morphology of Isoxys. (a) line drawing of idealized Isoxys illustrating known soft parts. (b) YPM IP 005804, Isoxys acutangulus from the Burgess Shale, British Columbia, Canada (Cambrian: Wuliuan) (credit: W. K. Sacco). (c) USNM PAL 189170, Isoxys longissimus from the Burgess Shale, British Columbia, Canada (Cambrian: Wuliuan). Image courtesy of the Smithsonian Institution (EZID: http://n2t.net/ark:/65665/m372f2a644-97c3-441c-87e2-24b1dccb2e8c, credit: Xingliang Zhang). Abbreviations: as, anterior spine; en, endopod; ex, flap like exopod; ey, eye; g, gut with paired diverticulae; ps, posterior spine; ra, raptorial appendage. (Online version in colour.)

Figure 3.

Principal component analysis of results of EFA conducted on the outlines of 11 species of Gnathophausia, 20 Isoxys, 1 Surusicaris and 6 Tuzoia. Convex hulls indicate optimum four groupings as recovered by clustering analysis. Labelled Isoxys species chosen for subsequent hydrodynamic analysis. (Online version in colour.)

Figure 4.

Drag polars (plot of Cd against Cl) of taxa analysed at Re = 255 (0.75 body lengths per second for an animal 25 mm long). Each point corresponds to a single simulation at a different angle of attack. Vertical bars show range of lift coefficients. Note that flow was unsteady for Isoxys zhurensis at Re = 255, and so no quantitative lift or drag coefficients were recorded. Drag polars at faster flow speeds and raw data presented in electronic supplementary material, S3. (Online version in colour.)

Figure 5.

First known appearance in the fossil record of metazoans that impacted the biological pump. Circle colour denotes preservation style. Fossils with more than one preservation style indicated with split circles, with the preservation style that provided the oldest evidence on the left of the circle. Abbreviations: Drum., Drumian; Guz., Guzhangian; Wul., Wuliuan. (Online version in colour.)