Microbial decay analysis challenges interpretation of putative organ systems in Cambrian fuxianhuiids

Abstract

The Chengjiang fossil (Cambrian Stage 3) from Yunnan, southern China is renowned for its soft-tissue preservation. Accordingly structures in fuxianhuiids, radiodontans and great appendage arthropods have been interpreted as the nervous and cardiovascular systems, including brains, hearts and blood vessels. That such delicate organ systems survive the fossilization process seems remarkable; given that this mode of preservation involves major taphonomic changes, such as flattening, microbial degradation, chemical alteration and replacement. Here, we document a range of taphonomic preservation states in numerous articulated individuals of We suggest that organic (partly iron mineral-replaced) bulbous structures in the head region, previously interpreted as brain tissue, along with sagittally located organic strands interpreted as part of the cardiovascular system or as nerve cords, may be better explained as microbial biofilms that developed following decomposition of the intestine, muscle and other connective tissues, forming halos surrounding the original organic remains.

Proclivity of nervous system preservation in Cambrian Burgess Shale-type deposits

“…Furthermore, Opabinia demonstrates that even a fossilized microbe-filled gut tract retains an important degree of morphological fidelity, for example, the presence of a J-shaped anterior curvature [63][64][65] (figure 6), which rules out the potential misinterpretation with neurological features such as the oesophageal foramen. These comparisons strengthen the interpretation that Alalcomenaeus from the Pioche and Marjum Formations, and by inference also Chengjiang [22], contain legitimate remains of the CNS whose complex morphology cannot be explained as the result of microbial activity within the body cavity (sensu [36,62]).…”

“…The availability of three specimens of Alalcomenaeus indicates that preservation of the CNS in this taxon is indeed repeatable, as also exemplified by the presence of multiple individuals with nervous tissues in Odaraia alata [24] and Waptia fieldensis [28][29][30] from the Burgess Shale, Fuxianhuia protensa from Chengjiang [25], and Chengjiangocaris kunmingensis from the Xiaoshiba biota [27]). The criticism of bilaterally symmetrical dark compressions exhibited by some Burgess Shale-type fossils is based on the argument that these compressions are not internal organs, but instead the remains of decay-related microbial films within body cavities [36]. The propagation of gut microbes within decaying carcasses has been thoroughly documented by laboratory experiments on the brine shrimp Artemia [62], which adequately explains the regularly spaced, paired subtriangular features repeatedly observed in the trunk of some Burgess Shale taxa, such as Opabinia [62,63], Surusicaris [57], Waptia [30] and Yawunik [54].…”

“…Although the microbial film hypothesis [36] offers a plausible alternative to the interpretation of problematic internal features observed in exceptionally preserved fossils, its ability to closely replicate delicate and complex structures should not be overestimated. In taphonomic experiments of ecdysozoans, decay microbes propagate within the cavities of the carcass, ultimately filling most of the loosened cuticular sac [34,35,62].…”

Canadia spinosa and the early evolution of the annelid nervous system

“…However, the interpretation of these features is not without controversy, and they have alternatively been identified as decayed remains of internal features ( 5 ) or as the result of differential shrinkage of internal features relative to the cuticle during decay ( 6 ), particularly in ecdysozoans. A major caveat of this view is that decay resistance is an imperfect predictor of preservation potential and that features preserved in fossil specimens do not always mirror decay stages of living analogs ( 7 ).…”

Biogenic Iron Preserves Structures during Fossilization: A Hypothesis

“…[ 18–20 ] These experimental results have consequently given rise to contrasting conceptual frameworks in the paleontology and evolutionary biology communities. [ 21–23 ] Although vital to constraining preservation pathways, [ 23 ] experimental decay data should be interpreted carefully and not projected directly onto enigmatic features in the geological record because fossils are not degraded carcasses and decay resistance is an imperfect indicator of fossilization potential. [ 24 ] Currently, there is no model accounting for the preservation of a specific labile tissue in a specimen where other more resistant tissues are completely absent.…”