Neotaphonomic characteristics of vertebrate site formation in underwater caves

This study establishes a benchmark taphonomic framework for underwater caves by demonstrating that submerged vertebrate remains generally exhibit superior preservation compared to dry cave deposits, yet display distinct biological modifications like cyanobacterial tunnelling and surface corrosion driven by light availability and associated microbial activity.

The Gist

Imagine you have a time machine that doesn't just travel through time, but also through water. This paper is about what happens to bones when they end up in underwater caves, compared to when they just sit on dry land.

The researchers are like underwater detectives, trying to figure out how to read the "story" written on bones to understand if they were buried in water or on land, and how long they've been there. They used a special trick: they took modern animal bones (like cow, sheep, and rabbit bones) that people had accidentally or intentionally thrown into two underwater caves in South Australia, and compared them to bones left on the dry surface of the same caves.

Here is the breakdown of their findings, using some everyday analogies:

1. The "Wet" vs. "Dry" Wardrobe

Think of the bones as clothes.

• The Dry Bones (Land): When bones sit on dry land, they get "sunburned" and "cracked" by the wind and sun. They tend to flake off in layers, like old paint peeling off a wall. They also get chewed on by rats or gnawed by other animals.
• The Wet Bones (Underwater): These bones are like clothes left in a gentle, constant rain. They don't flake off; instead, they tend to delaminate (peel apart like the layers of an onion) because they get soggy and then dry out unevenly. They are generally better preserved and less broken than the dry ones, but they get "soft" and mushy, making them fragile to touch.

2. The "Graffiti" on the Bones

Just like a wall gets graffiti, bones get "stains" and "etchings" from their environment.

• The Black Stain: In the underwater caves, the researchers found a distinct black stain on the bones. But here's the twist: it only appeared on the side of the bone facing the light! It's like a sunburn for bones. The "sun" in a cave is actually just the light coming from the entrance. Where the light hits, tiny living things (like algae and bacteria) grow and leave a black mark. Where it's dark, the bone stays clean.
• The "Target" Etching: The underwater bones had a weird, new kind of scratch that looked like a bullseye or a target (concentric circles). The researchers don't know exactly what made these yet, but they only found them underwater. It's like finding a unique fingerprint that says, "I was definitely underwater."

3. The Microscopic "Termite" Attack

The researchers looked at the bones under powerful microscopes to see what was happening inside the bone structure.

• Dry Bones: Inside the dry bones, the damage looked like a chaotic mess of tunnels, similar to termites eating wood from the inside out.
• Wet Bones: Inside the wet bones, they found a very specific type of tunneling caused by cyanobacteria (a type of blue-green algae). These tunnels are like tiny, straight tunnels drilled by a microscopic drill bit, starting from the outside edge and going inward. This is a "signature" of underwater life.

4. The "Light Switch" Theory

The biggest discovery is about light.
Imagine the underwater cave as a long hallway with a light switch at the entrance.

• Near the entrance (The "Twilight Zone"): There is enough light for plants and bacteria to grow. This is where the black stains, the "target" etching, and the specific algae tunnels happen. It's an active zone where nature is busy modifying the bones.
• Deep in the cave (The "Dark Zone"): Once you go deep enough that no light reaches, the "biological party" stops. The bones there are pristine, untouched by the algae or the black stains. It's a passive zone where the bones just sit quietly.

Why Does This Matter?

This study is a user manual for underwater archaeology.

• For Archaeologists: If they find a bone with black stains and "target" etching, they know it was underwater and exposed to light. If they find a bone with flaking layers and rat bites, they know it was on dry land.
• For Climate History: These caves often fill and empty with water as sea levels rise and fall over thousands of years. By looking at these "signatures" on the bones, scientists can tell exactly when the water was high and when it was low, helping us understand past climate changes.

In a nutshell: This paper teaches us that water doesn't just preserve bones; it writes a specific code on them using light, algae, and bacteria. If you know how to read that code, you can tell the story of where a bone has been, even if it's been underwater for centuries.

Technical Summary

1. Problem Statement

Underwater caves in karst environments often yield exceptionally well-preserved vertebrate remains, offering critical insights into archaeological and paleontological records. However, the site formation processes (taphonomy) of these environments remain poorly understood. Key challenges include:

• Time-Averaging: Stable, low-energy underwater conditions create unstratified, time-averaged deposits, making it difficult to reconstruct depositional histories.
• Lack of Actualistic Benchmarks: There is a scarcity of chronologically controlled studies comparing how bones modify in submerged (wet) versus dry cave environments.
• Methodological Limitations: Traditional excavation and recording methods are hindered by "silting out" and poor visibility in underwater caves.
• Knowledge Gap: It is unclear how specific factors like light availability, hydrology, and biological communities in underwater caves influence bone surface modifications (BSMs) and microstructural degradation (histotaphonomy) compared to terrestrial settings.

2. Methodology

The study employed an actualistic taphonomic framework using recently deposited (<250 years) domestic animal bones from two sites in Southeast South Australia:

• Study Sites:
  • Green Waterhole (GW): A doline collapse cave with both submerged conduits (wet) and a dry central area (dry).
  • Gouldens Sinkhole (GH): A deep, round sinkhole with submerged overhead environments and a historic access ramp.
• Sample Collection:
  • Total N = 231 specimens: 134 from wet contexts (submerged) and 97 from dry contexts (surface).
  • Contexts: Specimens were collected from varying depths (0.3m to 18.3m below surface) and dry surface areas.
• Chronological Control:
  • Radiocarbon Dating: 41 specimens were dated to establish two temporal groups: Decadal (<50 years, post-1955) and Centennial (50–185 years, 1841–1955). This allowed for the analysis of taphonomic changes over time.
• Analytical Techniques:
  • Macroscopic Analysis: Taxonomic identification (including ZooMS for 15 samples), skeletal element completeness, breakage indices, and recording of Bone Surface Modifications (BSMs) categorized by physical, chemical, and biological agents.
  • Chemical Analysis: Portable X-ray Fluorescence (pXRF) to analyze elemental composition of black staining.
  • Histotaphonomy (Microstructural Analysis):
    • 24 samples selected for undecalcified thin sections and Scanning Electron Microscopy (SEM).
    • Assessment of Oxford Histological Index (OHI), Bacterial Attack Index (BAI), and Cyanobacterial Attack Index (CAI).
    • Identification of specific bioerosion markers: Wedl-Tunnelling Type 1 (associated with cyanobacteria), Microscopic Focal Destruction (MFD), and radial microfractures.
  • Statistical Analysis: Chi-squared tests, Fisher's Exact tests, and Mann-Whitney U tests were used to compare wet vs. dry contexts and temporal groups.

3. Key Contributions

• First Benchmark Dataset: This is the first study to provide a comprehensive, chronologically controlled bone dataset specifically for reconstructing depositional histories in underwater cave environments.
• Differentiation of Wet vs. Dry Diagenesis: The study establishes distinct taphonomic signatures that allow researchers to distinguish between bones deposited in submerged versus dry cave conditions, even when stratigraphy is absent.
• Light-Driven Taphonomy: It identifies light availability as a primary driver of biological activity and subsequent bone modification in underwater caves, creating "active" (light-exposed) and "passive" (dark) taphonomic zones.
• Novel Microstructural Markers: It confirms the presence of peripheral cyanobacterial tunnelling (Wedl-Tunnelling Type 1) as a specific indicator of submerged burial, distinct from the terrestrial bacterial degradation seen in dry contexts.

4. Key Results

A. Macroscopic Preservation and Surface Modifications

• Overall Preservation: Wet contexts generally exhibited better preservation (higher skeletal completeness, less breakage) than dry contexts. Dry bones showed significantly higher frequencies of flaking and exfoliation, likely due to trampling and weathering.
• Delamination: Wet bones exhibited significantly higher rates of delamination (separation of the outer bone layer), a process exacerbated by the drying of waterlogged bones post-collection.
• Corrosion and Staining:
  • Wet Contexts: Characterized by surface corrosion (increasing with time), black staining with sharp margins, and biofilm/algae attack. A unique "circular target etching" (concentric rings) was identified exclusively in wet contexts.
  • Dry Contexts: Dominated by linear etching and pitting, often associated with root action from vascular plants.
  • Light Correlation: Black staining and biofilm growth in wet contexts were strongly correlated with light exposure (entrance zones), while deeper, darker zones showed less staining.
• Physical Damage: Wet bones were softer and more prone to plastic deformation and abrasion during collection, complicating the distinction between pre- and post-collection damage.

B. Histotaphonomy (Microstructure)

• Bioerosion Patterns:
  • Wet Bones: Dominated by peripheral cyanobacterial tunnelling (Wedl-Tunnelling Type 1). This tunnelling was restricted to the sub-periosteal (outer) region and did not typically penetrate deep into the cortex unless the bone was fractured.
  • Dry Bones: Dominated by terrestrial bacterial attack and Microscopic Focal Destruction (MFD) affecting the entire cortex, including sub-endosteal regions.
• Preservation: Despite surface corrosion, wet bones retained high histological integrity (high OHI scores) and birefringence, suggesting collagen preservation up to 180 years.
• Radial Microfractures: Contrary to some previous hypotheses, radial microfractures across secondary osteon cement lines were not observed in these relatively young (decadal/centennial) samples.

C. Temporal and Spatial Trends

• Time: Surface corrosion frequency increased significantly with time in wet contexts. However, the pattern of microstructural degradation (e.g., type of tunnelling) did not change significantly over the observed timescales (50–180 years).
• Depth/Light: The intensity of biological modification (staining, corrosion, cyanobacterial tunnelling) decreased with depth and distance from the cave entrance, correlating with reduced light availability.

5. Significance

• Reconstructing Depositional Histories: The identified markers (e.g., peripheral cyanobacterial tunnelling vs. terrestrial MFD; delamination vs. flaking) allow researchers to determine if a bone assemblage in an underwater cave was deposited during a wet (submerged) or dry phase. This is crucial for sites with fluctuating water tables due to glacial-interglacial cycles.
• Refining Chronologies: By distinguishing between wet and dry deposition, researchers can better narrow down the timing of depositional windows in time-averaged cave deposits.
• Understanding Cave Zonation: The study highlights that underwater caves are not uniform; they function as a gradient from "active" (light-exposed, high biological activity) to "passive" (dark, low activity) zones.
• Methodological Advancement: The study demonstrates the necessity of combining macroscopic BSM analysis with histotaphonomy to fully understand bone diagenesis in aquatic environments, as surface features alone may not reveal the full taphonomic history.

In conclusion, this paper provides a foundational framework for interpreting vertebrate remains in underwater karst systems, emphasizing that light availability and hydrological state are the primary determinants of bone modification patterns, offering new tools for archaeological and paleontological reconstruction.