Worms as wedges: Effects of sediment mechanics on burrowing behavior

Recent studies document linear elastic response of muddy marine sediments to load and deformation on temporal and spatial scales relevant to animal movement, with burrowers making openings for movement in such sediments by fracture. Cracks propagate through linear elastic solids in mode I (opening-mode crack growth) when the stress intensity factor (K-I) at the crack tip exceeds the material's fracture toughness (K-Ic). Fracture mechanics depend on material stiffness as well as fracture toughness, and we prepared a range of transparent gels that varied in stiffness and fracture toughness to assess the dependence of burrowing behavior on these material properties. When the polychaete Nereis virens elongated its burrow, it altered its body shape and behavior across these gels in a manner consistent with fracture mechanics theory. We modeled burrow elongation as stable, wedge-driven crack growth, and calculated that K-I values at the tips of the burrows reached K,, values of most gels without pharynx eversion and exceeded K-Ic when the pharynx was everted. In materials with higher fracture toughnesses, worms everted their pharynges to become thicker and blunter wedges, as predicted from simple wedge theory. In stiff materials with low toughness, worms moved their heads from side-to-side to extend crack edges laterally, relieving elastic forces compressing them and allowing them to maintain body shape more easily. This solution extends the crack in small increments that each require relatively little force. We introduce a dimensionless wedge number to characterize the relative importance of work to fracture the material and extend the burrow and work to maintain body shape against the elastic restoring force of the material. The mechanism of burrowing by crack propagation is utilized across a range of material properties found in natural muds, and variation in these properties strongly influences burrowing behaviors. These results demonstrate how quantifying the mechanical properties of muds can improve our understanding of bioturbation. On spatial and temporal scales relevant to burrower activity, variations in these properties may impact particle mixing by influencing burrower behavior.