Discovering the Pathway to Exceptional Fossil Preservation...During COVID

We unraveled the chemical reactions that could have allowed the exceptional preservation of spiders 22.5 million years ago using scanning electron microscopy, elemental maps, and Zoom.
Discovering the Pathway to Exceptional Fossil Preservation...During COVID

Most of the fossil record offers tantalizing snapshots of life through time rather than portraits of complete ecosystems. One commonly repeated aphorism is that less that one percent of one percent of the species that ever lived on Earth were fossilized. To maximize the chance of fossilization, an organism has to die in an environment that allows it to be quickly locked away from oxygen and buried in sediment, protecting it from decay and scavengers. Better still if the organism has biomineralized “hard parts”–bones, shells, teeth, horns–as these mineralized parts are easier to preserve than soft tissues like feathers, hair, skin, chitinous exoskeletons, which are much more likely to decay before fossilization can begin. However, more complete snapshots of entire ecosystems are preserved in Fossil-Lagerstätten, deposits of exceptional preservation where chemistry, sedimentology, and biology interact in such a way that soft-bodied organisms are preserved. Though relatively rare throughout geological time, these deposits provide much of what we know of soft bodied organisms and terrestrial life. Thus, given their importance as a source of information about life on Earth through time, it is crucial to better understand the specific conditions that allow this exceptional preservation, both to interpret the ecology of this ancient environment, and also potentially to act as a guide to find more such deposits. In this paper we examine the circumstances that led to the preservation of one such deposit, the Oligocene Aix-en-Provence Formation, a Fossil-Lagerstätte formed about 22.5 million years ago in what is now the South of France in a lake or brackish lagoon.

In its own way, this paper is the scientific version of a Lagerstätte (a Schreibenstätte if you will), as it is the product of unusual conditions. In May 2020, my collaborator at the University of Missouri, Jim Schiffbauer, collected chemical maps and whole-fossil SEM images of fossil spiders from the Aix-en-Provence Formation. Although he had just been able to open his lab up under tightly controlled pandemic conditions, mine was still closed, like all of the others on the University of Kansas campus. Even had mine been able to be opened, I would not have been able to go into the the lab: I was entering my second month of being home all day long with my then 6 and 8 year old daughters, who had not had school for 1.5 months and who, unbeknownst to me at the time, would not be returning to in-person school for another 15 months. Mine was not the only disrupted life, of course; pandemic conditions forced one collaborator to move 640 miles away to Kentucky while one retired and moved to France. Originally, this project was intended to be a traditional taxonomic description of the spider fossils preserved in the Aix-en-Provence Formation, but in Fall 2019, more or less on a whim, we put the spider fossils under the fluorescence microscope and were amazed to see that they autofluoresced. As a result, we sent the fossils off to Jim’s lab to better understand their chemistry, but the overall scientific goal was still to describe the taxonomy of these fossils. However, our plans, just like those of everyone else, had changed by May 2020. Each of us were at home, separated from the labs and the samples and each other. However, we did have these amazingly high resolution SEM images and chemical maps, images well suited for pouring over alone in our home offices or together on Zoom. In this way, data that were originally intended to be a side-note in the taxonomic study became the major focus of our research. We characterized every nanometer of those images, immersing ourselves in the microfossils and chemical relationships in a way that might not have occurred before lockdown.

That immersion in the chemical and microscopic analyses of fossil spiders is what allowed us to theorize a possible taphonomic pathway for the preservation of these spiders. First, fluorescence and scanning microscopy revealed that the fossils are associated with diatoms, a type of siliceous microalgae. As seen below, the matrix contains a dispersed collection of centric diatoms but the fossils themselves are covered with mats of pennate diatoms. Furthermore, microscopy revealed the presence of a black polymer on parts of the fossils. Coupling this with energy-dispersive X-ray spectroscopy allowed us to visualize the elemental distribution of the fossils and the surrounding matrix, revealing that the black polymer is composed of both carbon and sulfur. Putting all of these pieces together led us to posit that the diatom mats were crucial for this exceptional preservation. Diatoms excrete extracellular polymeric substances (EPS), a sticky chemically complex polymer rich in sulfur compounds. Thus, a diatom mat along the shore or in shallow water could entrap and entrain spiders and insects, creating an anoxic environment. However, the diatom mat would do more than just lock the organism away from oxygen, as the sulfur-rich composition of the EPS would promote microbial sulfate reduction, creating the chemical conditions necessary for sulfurization. Sulfurization, natural vulcanization, is an abiotic process initiated by the formation of sulfides by microbial sulfate reduction, and results in sulfur bridges crosslinking specific organic molecules, like carbonyl groups and carbon doubly bonded to carbon, which stabilizes and preserves those carbon polymers. Modern marine studies have shown this process to happen at low temperatures over hours to days, and it is thought that most of the organically bound sulfur found across the geosphere is a result of this process. Given these parameters, trapping a spider, which possesses a carbonyl-rich chitinous exoskeleton in EPS, a chemically complex mixture of sulfonate polymers, creates an environment particularly conducive to sulfurization. Intriguingly, many of the other Fossil-Lagerstätten found across the Cenozoic are also found in diatom rich environments, leading us to wonder if similar chemical reactions could have happened in lakes and brackish environments across the Cenozoic, preserving a tantalizing record of terrestrial life through a time period of great evolution and climate change.

Fossil Spider Overlain by Elemental Maps and Scanning Electron Microscopy Image
photograph of fossil spider with colorful chemical mapping data and microscopic image
Spider fossil from the Aix-en-Provence Formation with white box indicating location of scanning electron microscopy image and chemical map of sulfur (yellow) and silica (pink) seen in upper left. Together these reveal a black sulfur-rich polymer on the fossil and the presence of two kinds of siliceous microalgae: a mat of straight diatoms on the fossil and dispersed centric diatoms in the surrounding matrix.

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