Burrowing Behavior in Mud and Sand of Morphologically Divergent Polychaete Species (Annelida: Orbiniidae)

Abstract

Muddy and sandy sediments have different physical properties. Muds are cohesive elastic solids, whereas granular beach sands are non-cohesive porous media. Infaunal organisms such as worms that burrow through sediments therefore face different mechanical challenges that potentially lead to a variety of burrowing strategies and morphologies. In this study we compared three morphologically distinct polychaete species representing different clades in the family Orbiniidae and related differences in their burrowing behaviors and morphologies to their natural environments (mud or sand). Worms burrowed in transparent analogs for muds and sands, and kinematic analysis showed differences both among species and between materials. Leitoscoloplos pugettensis lives in mud and burrows by fracture, using its pointed head to concentrate stress at the tip of the burrow. Naineris dendritica lives in sand and uses its broader head that fluctuates in width over a burrowing cycle to decrease backward slipping in sand, potentially preventing burrow collapse. Orbinia johnsoni lives in sand and uses internal body expansions to pack sand grains, another mechanism to prevent burrow collapse. By combining data from species and materials to obtain a broad range of burrowing velocities, we show that burrowing worms control their velocity by increasing or decreasing their burrowing frequency rather than by altering cycle distance as shown previously for crawling earthworms. This study demonstrates how fairly small evolutionary divergences in morphologies and behaviors facilitate locomotion in environments with different physical constraints.

The biomechanics of burrowing and boring

“…Pointed anterior ends focus stress applied by the wider body to extend a narrow crack that is then expanded laterally by a peristaltic wave (Che and Dorgan, 2010). During and immediately following anterior crack extension, Leitoscoloplos pugettensis twists about its longitudinal axis, orienting its width, which exceeds its dorsoventral thickness, orthogonal to the crack edge (Francoeur and Dorgan, 2014). Twisting thus increases forces to extend the crack both anteriorly and laterally.…”

Burrowing by small polychaetes – mechanics, behavior, and muscle structure ofCapitellasp.

“…Capitella sp. exhibited no twisting behavior while burrowing that would be consistent with a torsion or twisting function of helical muscles, as in squid arms (Kier, 2012) or the behavior of the polychaete L. pugettensis (Francoeur and Dorgan, 2014). We cannot, however, eliminate the possibility that Capitella sp.…”

“…The muscle bands are usually located near the surface to increase the torsional moment (Kier, 2012 Periodic twisting behavior has been described for other polychaetes, e.g. the orbiniid Leitoscoloplos pugettensis (Francoeur and Dorgan, 2014), although the musculature driving the twisting behavior of L. pugettensis has not been explored. Connective tissue fibers can also form arrays of left-and righthanded helices around hydrostatic skeletons.…”

“…are contracted on alternate sides to achieve twisting or simultaneously either to elongate or shorten the body, we observed burrowing behavior for evidence of twisting and also measured helical muscle angle using confocal laser scanning microscopy (cLSM). Whereas twisting of the ovoid body shape of L. pugettensis facilitates burrowing by fracture by enabling greater displacement of the burrow walls (Francoeur and Dorgan, 2014), twisting of the more cylindrical body of Capitella sp. would be unlikely to facilitate burrowing by fracture.…”

Visualizing subsurface burrowing by the polychaete Alitta virens with particle image velocimetry

“…Dorgan et al (2007) developed a linear-elastic fracture mechanics model of burrowing based on observations of Alitta virens burrowing in gelatin. Cryolite has been used as a transparent analogue for sand (Josephson and Flessa 1972;Francoeur and Dorgan 2014). Unfortunately, no transparent analogs for sand have proven as effective as gelatin is for mud, and burrowing behaviors in sand are likely to differ from those in mud (Dorgan et al 2006) because cohesive sediments, such as mud, are mechanically different from noncohesive granular sediments, such as sand.…”