Cambrobranchus pelagobenthos, Yang & Kimmig & Cameron & Nanglu & Kimmig & Carle & Zhang & Yu & Abstract, 2024

Yang, Xianfeng, Kimmig, Julien, Cameron, Christopher B., Nanglu, Karma, Kimmig, Sara R., Carle, Danielle de, Zhang, Caixia, Yu, Mengxiao & Abstract, Shanchi Peng, 2024, An early Cambrian pelago-benthic acorn worm and the origin of the hemichordate larva, Palaeontologia Electronica (a 17) 27 (1), pp. 1-19 : 3-8

Cambrobranchus pelagobenthos gen. et sp. nov.

Figures 1 A-F, 2A-D, 3A-M, 4A-P, 5

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Type material. Holotype, YKLP14443 ( Figure 1 A- C, Appendix 1) from the Yu’anshan Member , Chiungchussu Formation , Cambrian , Epoch 2, Stage 3, Wutingaspis – Eoredlichia Biozone, on the eastern shore of Dianchi Lake , near Kunming, ~ 24 km northwest of Chengjiang County, China (Repository: YKLP) . Paratypes, YKLP14529–14537 , 14543 , 14544 ( Figures 1 D-F, 3A-H, Appendix 1) .

Other specimens. YKLP 14538–14540, 14542, 14545–14568 ( Figure 3M, Appendix 1).

Diagnosis. An enteropneust possessing a tripartite vermiform body consisting of proboscis, collar, and trunk. Proboscis approximately two times longer than wide; collar approximately two times longer than wide. A series of gill and tongue bars (GB+TB) accounting for 1/3–1/2 of the length of the trunk. The trunk is usually U-shaped or sinuous. Gut is straight with a post-anal organ structure. Indirect development with a tornaria larva.

Etymology. Genus name Cambro, for the period (Cambrian) in which the fossils are found; branchus for gills. Species name pelagobenthos (Latin) , for the lifestyle.

Type locality and horizon. Bottom 5 cm of the Haiyan Lagerstätte (Yang et al., 2021), Yu’anshan Member , Chiungchussu Formation , Cambrian , Epoch 2, Stage 3, Wutingaspis – Eoredlichia Biozone, on the eastern shore of Dianchi Lake , near Kunming, ~ 24 km northwest of Chengjiang County, China .

Description. Specimens are entirely soft-bodied and typically preserved as two-dimensional compressions. Body is tripartite, divided into proboscis, collar, and trunk. Specimens range from 500 μm to 33 mm in total length. The outer surface of the trunk preserves GB+TB, along with gill pores. There is an ovoid post-anal organ. The extension of GB+TB extends to one third or half of the trunk ( Figure 1 D-F, Appendix 1). The post-anal organ of a few specimens is adhered to unidentified biological fragments (Appendix 1). In some cases, individuals are found in clusters on a single slab (Appendix 1), co-occurring with tornaria larvae ( Figure 3A, C) and numerous juveniles ( Figure 3 EH, M).

The proboscis is well-preserved in almost all specimens, excluding tornaria, and is usually contracted, the exception being the YKLP14443 and YKLP14534 ( Figure 1A, Appendix 1) where it is extended. The proboscis is conical to cylindrical in shape ( Figures 1 A-F, 2A-D, 3E-H, M, Appendix 1). There is an axial zone within the proboscis coelom ( Figures 2A, 3M, Appendix 1) and at its anterior, an irregular elliptical region with a slight bulge, usually darker or more reflective than its surroundings ( Figure 3M, Appendix 1). The length of this major axis varies from 0.1 mm to 0.4 mm. The structure is herein interpreted as kidney–heart–stomochord complex (KHS) ( Figures 1 A-F, 2A-D, 3E-G, M, Appendix 1), as it is in the same area as the KHS in extant enteropneusts ( Balser and Ruppert, 1990) and fossil species from the Cambrian Burgess Shale (Caron et al., 2013; Nanglu et al., 2016, 2020a).

A 360-degree collar annulation with a raised outline attaches to the anterior of the trunk. The holotype collar is twice as long as wide ( Figure 1 A- C), and the length to width ratio of the proboscis, collar, and trunk are 2.5, 1.25, and 9, respectively (Appendix 1). Collar ridges are discernable at the anterior and posterior margins (Appendix 1), and many transversally corrugated bands are preserved. There are at least six rows of corrugated bands in specimen YKLP14529. The bands can also be found in some of the juvenile specimens ( Figure 3 E-H, M).

The dorsal branchial-pharynx region of the trunk is comprised of thick and thin gill bars alternating, herein interpreted as the GB+TB. Few of the gill slits have been completely exposed due to the taphonomy and possible ecology of the animals, but in specimen YKLP14545 (Appendix 1), a laterally compressed adult, there are about five sets of GB+TB for nearly every 500 μm (Appendix 1). The GB+TB are paired and symmetrically arranged on either side of an epibranchial ridge (EBR) ( Figure 1 D-F, Appendix 1). The gill slits are defined by gill bars and connect to the outside gill pores by atrial cavities. At least two to four gill pores can be identified in our collection ( Figure 3H, L, Appendix 1). The parabranchial ridges (PR) merge posteriorly ( Figure 1 D-F, Appendix 1). A single pair and serial pairs of GB+TB are well-preserved in YKLP14568 and YKLP14545, respectively (Appendix 1). Some relatively well-preserved GB+TB can be discerned in YKLP14562–14563, 14565–14567 (Appendix 1). The post pharynx region is a simple tube and best preserved in YKLP14565–14566 ( Figure 1 D-F, Appendix 1).

Digestive tract: The digestive system of C. pelagobenthos consists of a mouth, an enlarged pharyngeal area, an oesophageal organ (OO), a posterior intestine, and an anus. The mouth is ventrally located near the most anterior part of the collar ( Figures 1A, 3M, Appendix 1). The pharyngeal region extends from one third to almost half the length of the trunk ( Figures 1 D-F, 2A-B, Appendix 1) and preserves an end-pharyngeal pouch ( PH) at the anterior end (Appendix 1). A post-pharyngeal ovoid structure is visible in several specimens (Appendix 1) that is here interpreted as the OO, like the one present in other Cambrian and extant enteropneusts (Caron et al., 2013; Nanglu et al., 2016, 2020a). The OO is followed by the intestine, which terminates in the anus. The anus is rarely preserved but appears to be non-terminal, followed by a post-anal organ (PAO) of roughly ovoid shape. The length of the post-anal organ ranges from 57 μm in juvenile specimens to 454 μm in the largest adult specimen. It is present in several specimens ( Figures 2 A-B, 3M, Appendix 1) and is sometimes preserved with three-dimensional relief ( Figure 2 AB, Appendix 1).

Ontogeny and larval development: Two potential larval specimens have been identified ( Figures 3 A- D, 4), based on their morphology and compared with modern tornaria. There are other potential larvae present, but the preservation quality of these specimens prevents assignment. The specimens co-occur with juvenile, sub-adult, and adult specimens (Appendix 1), which is common among extant long-lived planktotrophic larva, including tornaria, which routinely settle in the adult sedimentary habitats (Flint and Kalke, 1986; Nielsen and Hay-Schmidt, 2007). The first ( Figure 3 A-B) is oval shaped, 1.5 mm long, showing the posterior ciliated telotroch swimming band. An outline of the larval body appears above the telotroch, potentially showing a ciliated feeding band and dark apical organ ( Figure 3A). The second ( Figure 3 C-D) is 1.6 mm in length, in anterior view, with a telotroch and feed bands, gut, and a retracted apical organ comparable to extant analogues that characterize the tornaria of modern acorn worms, including Schizocardium ( Figure 3N), Glandiceps , and ptychoderid species (Urata and Yamaguchi, 2004; Urata et al., 2014; Gonzalez et al., 2017, 2018).

Four additional fossils are interpreted as recently metamorphosed early juvenile develop-

YANG ET AL.: ORIGIN OF THE HEMICHORDATE LARVA mental stages (cf. Urata and Yamaguchi, 2004) ( Figure 3 E-H). The specimens show differentiation into a tripartite body with an elongated conical proboscis, collar, and trunk. The trunk is comparatively short with respect to that of adult specimens. YKLP14549 ( Figure 3H) represents an early juvenile specimen with at least two pairs of preserved oval-shaped gill pores (GP1 and GP2). Its length is 1.8 mm, and the position of the gill pores is like that of modern acorn worms (Urata and Yamaguchi, 2004; Urata et al., 2014).

Another seven specimens represent juveniles ( Figure 3M, Appendix 1). They are fully developed and morphologically comparable to extant juvenile specimens. The PAO is comparable to extant harrimaniid acorn worms ( Figure 3M), a probable homologue to the pterobranch stalk. The trunk of the juveniles has a length of ~ 1.6 mm in YKLP14551 ( Figure 3M). Those of juvenile worms to adults range from 2.2 mm to 33 mm long ( Figure 1 A-F, Appendix 1). A reconstruction of the different metamorphic stages can be seen in Figure 5 .

Remarks. Maletz (2019) reported the presence of pterobranchs from the Fortunian (Stage 1; Epoch 1). This suggests that pterobranchs and enteropneusts were already differentiated at that point, and that Cambrobranchus pelagobenthos may not represent the most basal enteropneust.