To further elucidate the possible biomechanical role of the outer
helicoidal region, we performed qualitative fracture experiments: high
load indentation was used to induce cracking and the sample surface was
examined in SEM (Figure 6). Indents placed in the striated region (along
the fiber axis, transverse section) require a fairly high load
(\(\sim\)1000 mN) to induce widespread damage: cracks follow a rather
straight path and spread radially in the matrix between fiber stacks
(Figure 6A). A central remark is that all cracks going towards the
highly mineralized region are stopped by the outer helicoidal
arrangement (Figure 6B and Figure S10 ). This is consistent with
the extensive delamination-based damage observed in transverse sections
(Figure 2A) and confined within the striated region by the inner and
outer twisted plywood. The damage observed in Figure 2A was not induced
by indentation but, most likely, by sample preparation. Specifically,
sample dehydration and related shrinkage are possible sources of local
cracking. Since mineral is believed to replace water, the amount of
dehydration (and shrinkage) should be higher in STR than in HMR (which
is more mineralized and therefore should contain less water). At the
same time, cracks were not observed in the OHR and IHR, which have a
comparable degree of mineralization than STR but helicoidal arrangements
preventing crack growth. A comparable damage behavior has been reported
for the uropod back spike, which has a similar multilayered
microstructure, but lacking the external highly mineralized region[42]. Indents performed in the highly mineralized
region require smaller loads (i.e., 50 - 500 mN) to generate extensive
cracking. In this heterogeneous region, a relevant observation is that
damage is more likely observed far from the transition region, which is
also the most compliant zone of the highly mineralized region. Indeed,
indents placed in the vicinity of this transition region either do not
cause cracks (Figure 6C) or induce damage running parallel to the
transition region and its lamella (Figure 6D). Remarkably, no cracks are
observed crossing the interface between the highly mineralized and the
outer helicoidal region. Typical high-load indentation curves a for the
highly mineralized region (HMR) and for the less mineralized but highly
anisotropic region (STR) are shown in Figure S11 . HMR featured
a characteristic pop-in event (highlighted by the arrow) associated with
sudden damage beneath the contact surface. Conversely, the indentation
curve of STR is free from pop-in events, indicating a more progressive
damaging behavior. The tiny dimension of the OHR (less than 10 μm in
width) precluded a quantitative assessment of the fracture toughness of
this region as previously done for the impact surface of both spearer
and smasher stomatopods [33,35]. Nevertheless, our
indentation-based fracture study proofs the critical role of the OHR for
decoupling damage mechanisms between HMR and STR regions. A closer
examination of the surface of a fractured spike highlights the damage
behavior of the regions from a different perspective (Figures 6E and F).
There is a clear transition between the rather straight fractured
surface of the highly mineralized region and the much rougher surface at
its interface with the outer helicoidal region. Inside the latter,
individual lamellae can be seen, suggesting a plausible role in crack
deflection and a corresponding switching from a more brittle to a more
ductile damage behavior. Furthermore, between the fiber beds of the
outer helicoidal region, unbroken pore canals are present. As in
decapods crustaceans [44], canals of the
stomatopods also contain fibers [36] that may act
as bridges between the chitin-protein fibers beds, possibly enhancing
fracture resistance [47].