Scaling of the hydrostatic skeleton in the earthwormLumbricus terrestris

Abstract

The structural and functional consequences of changes in size or scale have been well studied in animals with rigid skeletons, but relatively little is known about scale effects in animals with hydrostatic skeletons. We used glycol methacrylate histology and microscopy to examine the scaling of mechanically important morphological features of the earthworm Lumbricus terrestris over an ontogenetic size range from 0.03 to 12.89 g. We found that L. terrestris becomes disproportionately longer and thinner as it grows. This increase in the length to diameter ratio with size means that, when normalized for mass, adult worms gain ~117% mechanical advantage during radial expansion, compared with hatchling worms. We also found that the cross-sectional area of the longitudinal musculature scales as body mass to the ~0.6 power across segments, which is significantly lower than the 0.66 power predicted by isometry. The cross-sectional area of the circular musculature, however, scales as body mass to thẽ 0.8 power across segments, which is significantly higher than predicted by isometry. By modeling the interaction of muscle crosssectional area and mechanical advantage, we calculate that the force output generated during both circular and longitudinal muscle contraction scales near isometry. We hypothesize that the allometric scaling of earthworms may reflect changes in soil properties and burrowing mechanics with size. KEY WORDS: Scaling, Allometry, Ontogeny, Annelid, Burrowing INTRODUCTIONBody size plays a pivotal role in the structure and function of all organisms. Size affects how an organism interacts with its environment as well as the processes needed for survival (Vogel, 1988). Size also imposes physical constraints on organisms, with fundamental effects on organismal design (Schmidt-Nielsen, 1997). A range of important traits change as a function of body size, including: geometry, metabolic rate, kinematics, mechanics and even lifespan. As a consequence, almost every facet of an organism's life may be influenced by its size, including its physiology, morphology, ecology and biomechanics (Schmidt-Nielsen, 1984;Quillin, 1999;Vogel, 2013;Biewener, 2005;Hill et al., 2012). Scaling, the changes in form and function due body size, has been studied primarily in the vertebrates and in some arthropods (e.g. Schmidt-Nielsen, 1997;Biewener, 2005;Nudds, 2007;Chi and Roth, 2010). The effects of scaling on soft-bodied animals have, however, received relatively little attention. The aim of this study was to use histological and microscopic techniques to examine the effects of size and scale on components of the hydrostatic skeleton of an iconic soft-bodied animal, the earthworm.

Differences in scaling and morphology between lumbricid earthworm ecotypes

“…We also found significant interspecific and ontogenetic differences in scaling, consistent with our hypotheses (Kurth and Kier, 2014). Our results demonstrate that many aspects of the hydrostatic skeleton of earthworms develop in different ways between species, reflecting the ecological context of the organism.…”

“…In previous work, we showed that the burrowing earthworm Lumbricus terrestris becomes relatively thinner during growth and shows additional allometric changes in the musculature (Kurth and Kier, 2014). We hypothesized that these allometries may help to compensate for changes in strain hardening with growth.…”

“…The physical characteristics of soil may impose size-dependent constraints on burrowers (Dorgan et al, 2008;Che and Dorgan, 2010;Kurth and Kier, 2014). For example, many soils exhibit strain hardening, in which the modulus of compression (stiffness) of the soil increases with increasing strain (Chen, 1975;Yong et al, 2012;Holtz et al, 2010).…”

“…Hatchling worms may avoid the strain hardening effect as a result of the relatively small volume of soil they must displace during burrowing. Adult earthworms, however, are often several times longer and wider than hatchlings and must create wider burrows in order to accommodate their bodies (Gerard, 1967;Quillin, 2000;Kurth and Kier, 2014). The formation of new burrows is common when conditions change or resources become scarce, forcing large worms to encounter and overcome strain hardening (Evans, 1947;Gerard, 1967).…”

“…The formation of new burrows is common when conditions change or resources become scarce, forcing large worms to encounter and overcome strain hardening (Evans, 1947;Gerard, 1967). Thus, as a burrower grows there may be a selective advantage to becoming relatively thinner to mitigate the strain hardening effect (Piearce, 1983;Kurth and Kier, 2014).…”