Sophisticated digestive systems in early arthropods

Abstract

Understanding the way in which animals diversified and radiated during their early evolutionary history remains one of the most captivating of scientific challenges. Integral to this is the 'Cambrian explosion', which records the rapid emergence of most animal phyla, and for which the triggering and accelerating factors, whether environmental or biological, are still unclear. Here we describe exceptionally well-preserved complex digestive organs in early arthropods from the early Cambrian of China and Greenland with functional similarities to certain modern crustaceans and trace these structures through the early evolutionary lineage of fossil arthropods. These digestive structures are assumed to have allowed for more efficient digestion and metabolism, promoting carnivory and macrophagy in early arthropods via predation or scavenging. This key innovation may have been of critical importance in the radiation and ecological success of Arthropoda, which has been the most diverse and abundant invertebrate phylum since the Cambrian.

Hallucigenia's head

“…Although pharyngeal teeth and circumoral mouthparts have been reported in other Cambrian lobopodians 7,8 as an ancestor of living onychophorans (com monly known as velvet worms), so the find ing of H. sparsa mouthparts suggests that the absence of circumoral elements and pharyn geal teeth in extant onychophorans is probably the result of secondary loss. Thus, this com bined structure is now reported for all major ecdysozoan groups.…”

Molaria (Euarthropoda) from the Sirius Passet Lagerstätte (Cambrian Series 2, Stage 3) of North Greenland

“…The preservational and diagenetic history of the Sirius Passet Lagerstätte is complex (Budd 1997(Budd , 1998(Budd , 2011Conway Morris & Peel 2008;Peel et al 2013;Stein et al 2013;Vannier et al 2014;Strang et al 2016a, b;Peel 2017) and excellent preservation was not extended equally to all. Each of the 10-15 arthropod taxa currently known has its own preservational history, with internal axial structures and distal portions of antennulae and other limbs particularly subject to variable preservation.…”

“…Sirius Passet taxa with originally calcareous exoskeletons often retain high relief, the latter including the trilobite Buenellus higginsi Blaker, 1988, the armoured Halkieria evangelista Conway Morris &Peel, 1995 andhyoliths (Peel 2010), as well as individual spicules from the diverse assemblage of sponges (Botting et al 2015, Botting & Peel 2016. Burgess Shale style preservation occurs at certain horizons at Sirius Passet (Vinther et al 2011a, b), but a characteristic feature of many, but not all, arthropods and lobopodians from the Sirius Passet Lagerstätte is the three-dimensional preservation of the axis and digestive tract resulting from early post-mortem mineralization (Budd 1997(Budd , 2011Vannier et al 2014;Strang et al 2016a;Peel 2017).…”

“…The three-dimensional preservation indicates early post-mortem mineralization that may reflect the mediating role of endogenous bacteria in phosphatization within the digestive system, but phosphorus and calcium also may have been stored within the digestive tract during life (Watabe 1989, Butterfield 2002, Butler et al 2015, Zacaï et al 2016, Strang et al 2016a, Peel 2017. Vannier et al (2014) identified phosphates just in the mineralized digestive tract of the lobopod Pambdelurion while silicified muscle fibres were reported by Budd (1998Budd ( , 2011 More than 1700 specimens of the isopygous arthropod Campanamuta mantonae Budd, 2011 are known from Sirius Passet. Many display three-dimensional differential preservation of soft parts in the axial region, and muscle fibres, the gut and paired digestive glands have been recognized (Budd 2011).…”

Coprolites in mid-Cambrian (Series 2-3) Burgess Shale-type deposits of Nevada and Utah and their ecological implications

“…Specimens have been reported from the early Cambrian Paseky Shale of the Czech Republic (Mikuláš 1995), the early Cambrian Maotianshan Shale of China (Vannier & Chen 2005), the mid-Cambrian Kaili Lagerstätte of China (Lin et al 2010), and the mid-Cambrian of Sweden (Eriksson & Terfelt 2007). Despite this growing number of known fossilized coprolites in the Cambrian and the improved knowledge on digestive tracts and feeding habits of several Cambrian animals (Lerosey-Aubril et al 2012, Vannier 2012, Vannier et al 2014 it is often unclear what kind of animal(s) are the source of the coprolites. In most cases though, arthropods or worms are considered to be the producers (Mikuláš 1995, Vannier & Chen 2005, Shen et al 2014.…”