Experimental taphonomy of Artemia reveals the role of endogenous microbes in mediating decay and fossilization

Abstract

Exceptionally preserved fossils provide major insights into the evolutionary history of life. Microbial activity is thought to play a pivotal role in both the decay of organisms and the preservation of soft tissue in the fossil record, though this has been the subject of very little experimental investigation. To remedy this, we undertook an experimental study of the decay of the brine shrimp Artemia, examining the roles of autolysis, microbial activity, oxygen diffusion and reducing conditions. Our findings indicate that endogenous gut bacteria are the main factor controlling decay. Following gut wall rupture, but prior to cuticle failure, gut-derived microbes spread into the body cavity, consuming tissues and forming biofilms capable of mediating authigenic mineralization, that pseudomorph tissues and structures such as limbs and the haemocoel. These observations explain patterns observed in exceptionally preserved fossil arthropods. For example, guts are preserved relatively frequently, while preservation of other internal anatomy is rare. They also suggest that gut-derived microbes play a key role in the preservation of internal anatomy and that differential preservation between exceptional deposits might be because of factors that control autolysis and microbial activity. The findings also suggest that the evolution of a through gut and its bacterial microflora increased the potential for exceptional fossil preservation in bilaterians, providing one explanation for the extreme rarity of internal preservation in those animals that lack a through gut.

Keywords: Cambrian explosion; bilateria; metazoa; palaeobiology; taphonomy.

Figure 1.

Generalized decay sequence in Artemia (a–g) and comparison to Burgess Shale-type fossils (h–i). (a) Undecayed specimen. (b) Thoracopods become matted. (c) Body and limbs (arrow) becomes opaque due to microbial activity. (d) Cuticle shrinks; some distal podomeres are disarticulated, cloudy appearance of limbs indicates internal biofilm. (e) Cuticle fails, internal biofilm is lost. (f) Cuticle disintegrates into fragments. (g) Only the unsupported gut remains. (h) Opabinia specimen (Burgess Shale, BC, Smithsonian National Museum of Natural History Washington DC, USNM 155600) showing the gut and associated microbial fabrics. (i) Enlargement of Opabinia gut area (Burgess Shale, BC, Geological Survey of Canada GSC 40251). Dark area, g gut; gf grey features corresponding to structures interpreted as gut diverticulae or limbs, bc lighter areas, body cavity. Scale bar: (a–c,i) = 2 mm, (d–g) = 1 mm, (h) = 10 mm. (Online version in colour.)

Figure 2.

Microbial activity during Artemia decay. (a) Hindgut of live Artemia. (b) Microbes (arrow) escape at midgut/hindgut boundary and migrate into haemocoel. (c) Cuticle filled with microbes forming a dense biofilm; (d) replacement of gut epithelium by microbial pseudomorph. bm, basement membrane; bf, biofilm; gc, gut contents; m, musculature surrounding gut. (e) Section of appendage filled with biofilm (reducing conditions). (f) Enlargement of (e). (g) Surface microbes at early stage decay. (h) Diverse microbial community after 28 days in closed conditions. Scale bar (a) 500 µm, (b) 250 µm, (c) 50 µm, (d) 20 µm, (e) 200 µm, (f) 10 µm, (g) 20 µm, (h) 300 µm. (Online version in colour.)

Figure 3.

Count data of decay experiments, six samples coded per interval. (Online version in colour.)

Figure 4.

Graphs of median decay stage at each recorded time interval, error bars indicate median absolute deviation per interval where value is greater than zero. (Online version in colour.)

Figure 5.

Biofilm associated with gut and internal body cavity with phosphatic mineral spheroids growing in situ. (a) Internal body cavity biofilm. (b) Gut-associated biofilm. Arrows indicate phosphatic spheroids. (c) Point EDX spectrum from mineralized spheroid, note distinct Ca, Mg and P peaks (not present in surrounding tissue) Au peak results from gold coating used for SEM imaging. Scale bar: (a) 20 µm and (b) 30 µm. (Online version in colour.)

Figure 6.

General model of decay in Artemia in open conditions.

Figure 7.

Hypothesized model of decay and pathways leading to exceptional preservation.