One size does not fit all: diversity of length–force properties of obliquely striated muscles

The tentacle longitudinal fibers produced high forces over an exceptional range of lengths (Fig. 6; Fig. S2). The ‘90% range’ (Lowy and Mulvany, 1973) is defined as the width of the active length–force curve at 0.9P0, and is a measure of plateau breadth. The 90% range for the tentacle (0.54L0 for the average relationship for the tentacle; Fig. 6) was 2–3 times greater than the 90% range typically found for cross-striated muscles. For example, the 90% range of bullfrog plantaris (0.19L0; Azizi and Roberts, 2010), mouse soleus (0.24L0; Askew and Marsh, 1998), carp jaw closers (0.13L0; Gidmark et al., 2013) and cockroach leg muscle (0.17L0; Ahn et al., 2006) is substantially narrower than observed for the tentacle longitudinal fibers. In fact, the tentacle has a larger 90% range than even the smooth muscle taenia coli from guinea pigs (0.47L0; Lowy and Mulvany, 1973).

We found no evidence that superelongation is a common trait among obliquely striated muscles in D. pealeii. Although the breadth of the length–force relationship varied among the squid muscles we examined, only one, the tentacle longitudinal muscle, demonstrated the broad length–force relationship and high degree of extensibility characteristic of superelongating muscles. Thus, superelongation seems to be more of an exception than a rule, at least within D. pealeii.

We found only mixed support for the prediction that the length–force relationship varies proportionately with the strain experienced by the muscle in vivo. The muscle fibers measured in the present study included those estimated to experience large (tentacle longitudinal; Kier, 1982; Kier and Van Leeuwen, 1997), intermediate (head retractor, mantle circular; Thompson et al., 2014, 2016) and short (funnel retractor, fin and arm transverse; Kier, 1982; Kier et al., 1989; Rosenbluth et al., 2010) excursions in vivo. The shape of the length–force curves observed for squid muscles may reflect their function in some cases but for others it is unclear. For example, the tentacle longitudinal fibers exhibited a broad active length–force curve and low passive forces, as we expected given the large in vivo strains of the tentacle stalk during the prey strike (Kier, 1982; Kier and van Leeuwen, 1997). Similarly, the fin transverse fibers likely undergo very little length change in vivo (Kier, 1989; Kier et al., 1989) and correspondingly have a narrow active curve and develop passive forces at short lengths. The funnel retractor, however, experiences low strains across a range of behaviors (Rosenbluth et al., 2010) yet has one of the broader non-tentacle length–force curves for D. pealeii (Fig. 6).

Four of the D. pealeii muscle preparations (transverse arm and fin fibers; longitudinal funnel retractor and head retractor fibers) could not be stretched much longer than L0 without either tearing or experiencing a permanent decrease in isometric force output. This in vitro mechanical behavior is inconsistent with superelongation. The muscular organs from which these preparations were derived all qualitatively felt stiffer and were less deformable than the tentacle stalks, when handled immediately post-mortem. It is possible that differences in connective tissue fiber quantity and arrangement (e.g. Di Clemente et al., 2021) and/or intrinsic differences in muscle fiber stiffness underlie the differences in extensibility we observed.

Regardless of the causes, the presence of such short descending limbs for the arm, fin, funnel retractor and head retractor muscles suggests that they operate predominantly along the ascending limb of the length–force curve in vivo. The measurement of muscle fiber strain during movement in soft-bodied invertebrates is particularly challenging given that their bodies and organs typically lack hard parts or other reference points that can be monitored during movement to reconstruct muscle strain, as for instance is done in vertebrate studies using X-ray reconstruction of moving morphology (XROMM) (Brainerd et al., 2010). Sonomicrometry can sometimes be used (see Thompson et al., 2014, for an example), if the in vivo and in vitro strains can be precisely correlated, but the documentation of the range of muscle strain during movement in soft-bodied invertebrates remains a significant gap in our understanding. Thompson et al. (2014) showed that the obliquely striated mantle circular muscles of D. pealeii operate primarily on the ascending limb of the length–tension curve as do other muscles, such as the cross-striated adductor muscles of the bay scallop Argopecten irradians (Olson and Marsh, 1993; Marsh and Olson, 1994), the wing depressor of the hawkmoth Manduca sexta (Tu and Daniel, 2004), the papillary muscles of mammals (Allen and Kentish, 1985; Layland et al., 1995), the atrial trabeculae of frogs (Winegrad, 1974), and human soleus muscles (Rubenson et al., 2012). Operating on the ascending limb has been suggested to allow cyclically active muscles to respond to a stretch by increasing their capacity to produce force, though at the cost of decreased work and power. In addition, operation on the ascending limb is hypothesized to provide non-neural mechanisms for regulating muscle excursion lengths during cyclical contractions (Rubenson et al., 2012; Tu and Daniel, 2004). Although it is unclear whether these hypotheses apply to the muscles we studied, the fins (Kier, 1989; Kier et al., 1989), funnel retractor (Rosenbluth et al., 2010) and head retractor (Thompson et al., 2016) are all involved in rhythmic movements during jetting and fin undulation.

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