Introduction
Feeding structures can be highly adapted to the preferred ingesta (i.e., food, particles on the food, substrate that the food is attached to). In molluscs, the radula is the structure that processes food/ingesta intake. It is a unique molluscan development and consists of a chitin membrane with embedded rows of teeth. The tooth morphology and the arrangement of teeth on the membrane can relate to the ingesta source (e.g., Solem, 1972, 1974; Steneck & Watling, 1982; Hawkins et al., 1989; Padilla, 2003; Ukmar-Godec et al., 2015; Krings et al., 2021b, 2021c, 2021d).
Even though the radula is constantly renewed by secretion in the posterior radular region (the “radular sac”) by over- and underlain epithelia (Runham, 1963; Runham & Isarankura, 1966; Mackenstedt & Märkel, 1987; Vortsepneva et al., 2022), the radular material properties are adapted during formation to reduce wear and/or structural failure induced by the specific ingesta source.
Structural failure can be reduced by the presence of mechanical property gradients (i.e., of the Young’s modulus) along each tooth. In polyplacophorans, limpets, or some gastropod taxa (e.g., some members of the Paludomidae and Nudibranchia), the radula needs to transfer high forces to solid surfaces (e.g., rocks) by scratching action or to hard structures of the prey (e.g., sponge spiculae) by piercing action. Here, each tooth shows pronounced gradients with the cusp as the hardest and stiffest region, followed by the stylus and finally the basis, as the softest and most flexible region (van der Wal et al., 1999; Weaver at al., 2010; Lu & Barber, 2012; Herrera et al., 2015; Krings et al., 2019, 2022c, 2022d, 2023; Pohl et al., 2020; Gorb & Krings, 2021). This allows teeth to bend and to either gain support from the next row of teeth, which redistributes the stress, or to deform and adjust to the prey item to avoid structural damage. These mechanical property gradients have their origin in the degree of tanning, the content of inorganics, the regional water content or the chitin fiber arrangement (e.g., Brooker & Shaw, 2012; Faivre & Ukmar-Godec, 2015; Joester & Brooker, 2016; Krings et al., 2021b, 2022d).
With regard to abrasion resistance, some taxa, like Polyplacophora and Patellogastropoda, incorporate high proportions of iron and silicon into their very thick tooth leading edge (i.e., the surface of the tooth that interacts directly with the ingesta) resulting in hard tooth cusps as adaptation to feeding on algae growing on stone (e.g. van der Wal et al., 1999; Wealthall et al., 2005; Shaw et al., 2009a, 2009b, 2010; Weaver at al., 2010; Saunders et al., 2011; Han et al., 2011; Lu & Barber, 2012; Wang et al., 2014; Barber et al., 2015; Krings et al., 2022c). High inorganic contents such as Ca or Si were also found on the leading edges (“leading surfaces”) of other gastropod taxa (e.g., some Paludomidae foraging on algae also growing on rock, and Nudibranchia foraging on Porifera as well. However, the coating was very thin in comparison to the leading edge of Polyplacophora, suggesting that these teeth resemble highly functional lightweight structures (Krings et al., 2022a, 2023). Teeth that come in contact with abrasive particles, like sand, were found to contain a thin layer with high content of Ca on all tooth surfaces, presumably to prevent high wear (Krings & Gorb, 2023a).
In this context, we here aim at unravelling the functional principles that reflect adaptation to the ingesta source in the radular teeth of the gastropod Gastropteron rubrum (Rafinesque, 1814) (Heterobranchia, Euopisthobranchia), which forages on Foraminifera (DeLaHoz et al., 2018). Members of these single celled protists have a cacliumcarbonate skeleton and thus represent a hard and abrasive ingesta. This is the first tooth analysis of a gastropod that mainly preys on this kind of food. First, the stomach content of the sea slug was documented under scanning-electron-microscopy (SEM) to gain insight into the food composition in detail. Then, the teeth were carefully documented unravelling the wear at the tooth cusps. The mechanical properties of the teeth were tested using nanoindentation technique to get insights on the functional adaptations of the radular apparatus. In the search for the origins of the mechanical properties in the teeth, we also investigated the material composition. The degree of tanning of the teeth was visualized using confocal laser scanning microscopy (CLSM), and the elemental composition were analyzed with energy-dispersive X-ray spectroscopy (EDS, EDX).