Early Cambrian origin of modern food webs: evidence from predator arrow worms

Abstract

Although palaeontological evidence from exceptional biota demonstrates the existence of diverse marine communities in the Early Cambrian (approx. 540-520 Myr ago), little is known concerning the functioning of the marine ecosystem, especially its trophic structure and the full range of ecological niches colonized by the fauna. The presence of a diverse zooplankton in Early Cambrian oceans is still an open issue. Here we provide compelling evidence that chaetognaths, an important element of modern zooplankton, were present in the Early Cambrian Chengjiang biota with morphologies almost identical to Recent forms. New information obtained from the lowermost Cambrian of China added to previous studies provide convincing evidence that protoconodont-bearing animals also belonged to chaetognaths. Chaetognaths were probably widespread and diverse in the earliest Cambrian. The obvious raptorial function of their circumoral apparatuses (grasping spines) places them among the earliest active predator metazoans. Morphology, body ratios and distribution suggest that the ancestral chaetognaths were planktonic with possible ecological preferences for hyperbenthic niches close to the sea bottom. Our results point to the early introduction of prey-predator relationships into the pelagic realm, and to the increase of trophic complexity (three-level structure) during the Precambrian-Cambrian transition, thus laying the foundations of present-day marine food chains.

Figure 1

Lower Cambrian and Recent chaetognaths. (a), (b), (d), (e) Protosagitta spinosa from the Chengjiang biota (Yu'anshan Formation, Ercaicun near Kunming, Yunnan Province, China, coll. Yunnan Institute of Geological Science, Kunming, no. Che-f-1001), general morphology and head. (c) Recent Sagitta hispida. (f) head of Sagitta nagae, Recent, Pacific Ocean (Suruga Bay, Japan), ventral view. Coloured areas (mainly iron oxide) represented by grey tones. an, anus; as, anterior septum; cf, caudal fin; co, collarette; fl, frontal lobe; gs, grasping spines; hd, head; ho, hood; in, intestine; lf, lateral fin; lp, lateral plate; m, mouth; mu, muscles; ne, neck; ov, ovary; ps, posterior septum; sv, seminal vesicle; ta, tail; te, teeth; tr, trunk. Scale bars, 5 mm in (a), (b), 1 mm in (c)–(e) and 200 μm in (f).

Figure 2

Protoconodonts from the lowermost Cambrian Kuanchuanpu Formation, Hexi Shaanxi Province, China (a)–(b) and Kuanchuanpu (c)–(d), both, and grasping apparatus of Recent chaetognaths (e)–(h).(a), (b) Protohertzina unguliformis, isolated element and natural cluster (coll. TU Berlin, no. He22-Re and He22-195, respectively). (c), (d) Mongolodus longispinus, cluster of five elements seen in different orientations (Kua125-166). (e) Sagitta nagae (base removed by NaOH dissolution). (f) Eukrohnia hamata, transverse section through grasping spine showing details of chitinous structure. (g), (h) Dissected cluster of grasping spines of Sagitta ferox and half-apparatus of Sagitta lyra. am, anterior margin; b, base; h, head; il, inner layer; ml, middle layer; ol, outer layer; pm, posterior margin; s, shaft. Protoconodonts were obtained, along with other small shelly fossils, by digestion of phosphatic carbonates in 10% buffered acetic acid and hand-picked from residues under the binocular microscope. Scale bars, 200 μm in (b)–(d), (g) and (h), 100 μm in (a) and (e), and 20 μm in (f).

Figure 3

Wall microstructure of Recent chaetognath grasping spines (a, b) and lowermost Cambrian protoconodonts (c, d), from the Kuanchuanpu Formation, Hexi, Shaanxi Province, China. (a) Eukrohnia hamata, three-layered chitinous structure. (b) Sagitta lyra, exfoliated distal part showing chitin fibrils. (c) Protohertzina anabarica showing fibrous structure of middle layer. (d) P. unguliformis, basal part showing inner and outer layers. cf, chitin fibrils; ic, inner cavity; il, inner layer; ml, middle layer; ol, outer layer. Scale bars, 5 μm in (a), 10 μm in (b) 20 μm in (c), and 100 μm in (d).

Figure 4

Facies reconstruction and distribution of protoconodonts over the Yang Tze Platform, South China, for the earliest Cambrian (Meishucunian Stage). Protohertzina anabarica, P. unguliformis and Mongolodus longispinus.