Mechanical behaviour and foraging
The mechanical properties of materials directly contribute to the mechanical behaviour of structures. The Young’s modulus (E) relates to the ability of a structure to transmit force (Bendsøe & Kikuchi, 1988; Bendsøe, 1989, 1995; Dumont et al., 2009) and its resistance to failure, as well as the structures’ mechanical behaviour while puncturing (e.g., Freeman & Lemen, 2007; for review on puncture mechanics see Anderson, 2018). The hardness (H) is the measure of the resistance to local plastic deformation induced by indentation or abrasion.
Some gastropod species (i.e., paludomid taxa) feeding on soft ingesta (i.e., algae growing on soft substrate like sand or mud) possess soft and more flexibles teeth (E ≤ 8 GPa, H ≤ 1 GPa) without clear and pronounced gradients in mechanical properties from the tooth basis across the stylus to the cusp (Gorb & Krings, 2021). These teeth are probably not capable of transferring high forces without structural failure, but possess an increased ability to deform, bend, and twist, which reduces the risk of breaking (Krings et al., 2021b, 2021c). Since all teeth within one row have similar mechanical properties, they probably also have a similar function (“monofunctional radula”; see Krings, 2020; Gorb & Krings, 2021).
Species foraging on the solid ingesta (members of Paludomidae foraging on algae covering rocks, Patellogastropoda, Fissurellidae, Polyplacophora) or have some interactions with hard ingesta (the nudibranch gastropods Felimare picta and Doris pseudoargusfeeding on Porifera with hard spiculae) possess harder and stiffer teeth reducing wear and structural failure. Each tooth shows pronounced gradients in both H and E: the cusp (especially the leading surface) is the hardest and stiffest part, followed by the stylus, and finally the basis with the softest and most flexible part (Weaver et al., 2010; Lu & Barber, 2012; Grunenfelder et al., 2014; Barber et al., 2015; Ukmar-Godec et al., 2017; Krings et al., 2019, 2022c, 2022d, 2023; Gorb & Krings, 2021). In the above mentioned taxxa, the tooth cusps puncture the ingesta or scratch across solid surfaces with the possible formation of local stress at the cusps, but without high degrees of wear or structural failure. The softer and more flexible stylus, together with the basis, provides flexibility and act as shock absorber against mechanical impacts (Herrera et al., 2015; Krings et al., 2019, 2022c, 2022d, 2023; Pohl et al., 2020; Gorb & Krings, 2021).
The dominant teeth of the so far investigated Polyplacophora are characterized by a very high inorganic content and the E values range from 30 to 130 GPa and H values from 4 to 12 GPa (Weaver et al., 2010; Grunenfelder et al., 2014; Krings et al., 2022c). In the highly mineralized dominant teeth of Patella vulgata(Patellogastropoda), E values from 52 to 150 GPa and H values of 3 to 7 GPa were detected (Lu & Barber, 2012; Barber et al., 2015). Less mineralized teeth are softer and more flexible: in the vetigastropodMegathura crenulata (Fissurellidae) E values of 16 GPa were determined (Ukmar-Godec et al., 2017). In the two investigated nudibranch species, where the inner structure of teeth also contained low inorganic content, Emax. values of 15 GPa and Hmax values of 0.9 GPa were found (Krings et al., 2023). Their thin leading surfaces were however significantly harder (Hmax = 2.3 GPa) and stiffer (Emax = 45 GPa) than the inner structure, due to high proportions of Si or Ca. The unmineralized teeth of paludomid gastropods foraging from solid surfaces were even softer and more flexible in comparison to the inner structure of the nudibranch taxa (H =~0.4 GPa and E =~8 GPa; see Gorb & Krings, 2021). However, here the neighboring teeth could interlock when loaded, leading to stress redistribution when in contact with the ingesta. This mechanical behaviour is prospered by the arrangement and geometry of teeth, the water-content and the material properties which enables the bending capacity (Solem, 1972; Hickman, 1980, 1984; Morris & Hickman, 1981; Padilla, 2003; Ukmar-Godec et al., 2015; Herrera et al., 2015; Montroni et al., 2019; Krings et al., 2020, 2021b, 2021c, 2021d, 2021e; Krings & Gorb, 2021).
In some solid substrate feeders (i.e., the nudibranch gastropodsFelimare picta and Doris pseudoargus ), the different teeth of each row had similar mechanical properties. Here, teeth probably also had similar functions (“monofunctional radula”; Krings et al., 2023). However, in other taxa, there were pronounced gradients within each transversal tooth row present, i.e. different tooth types had different mechanical properties. E.g., in some paludomid gastropods, the central teeth were the stiffest and hardest elements, followed by the lateral, and finally the marginal teeth (Krings et al., 2019, 2022d; Gorb & Krings, 2021). The central and lateral teeth are probably capable of loosening algae from rocks, whereas the marginal teeth rather collect loosened food particles in a complex motion of the buccal mass afterwards. Since teeth of one row probably had different functions, this type of radula was previously termed “multifunctional radula” (see Krings, 2020; Gorb & Krings, 2021).
The teeth of Gastropteron rubrum show mechanical properties that were comparable to Nudibranchia teeth. In G. rubrum , the large inner laterals are harder and stiffer than the smaller outer laterals, with the outermost being the softest and most flexible ones. This indicates that the different teeth might experience different loads during foraging. With regard to the tested regions, we found that the bases and the bulges are most flexible and soft. This suggests that the teeth can bend in anterior-posterior direction around their bases, probably adjusting to the sizes of different prey items. Additionally, teeth are probably capable of bending in lateral-medial direction with the bulges serving as cushions (see Figure 8). This mechanical behaviour was also observed when the radula was manipulated by tweezers: the radula could be folded around the groove towards medial. As consequence the teeth bent towards the center forming a groove. SEM documentation revealed that the degree of wear and structural failure decreased towards the radular sides. All of this suggests, that during feeding, the Foraminifera (and the sand particles) or Porifera parts are clamped between the inner laterals during folding along the groove (Figure 8C). During this, the softer and more flexible outer teeth could serve as cushions and supporting structures, which would render this radula to be multifunctional since teeth have different functions. Subsequently, the radula with the particles or Porifera parts is pulled into the mouth cavity. This system would allow G. rubrum to take in all kind of different ingesta sizes, since its radula could easily adapt to prey shapes.
Besides the prey items, we detected various sand particles in the intestine. This indicates, that individuals of G. rubrum do not feed selectively, but instead probably feed on the sand surface and take everything randomly in. Since prey from the distal region of the intestine was more brittle and fractured than the prey extracted from the proximal regions, digestion in G. rubrum potentially involves acidic liquids.