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Radular teeth as models for the improvement of industrial cutting devices
Abstract
Limpets Gastropoda and chitons Polyplacophora feed on epi-and endolithic organisms by means of the radula, a specialized feeding apparatus located in the mouth cavity. The radula owes most of its abrasive capability to the presence of numerous mineralized teeth. Here we report on the shape, internal structure, wearing pattern, feeding position, and distribution of hardness and elastic properties of these teeth in an attempt to generate ideas for the innovation of industrial cutting devices. The teeth remain sharp during their entire working-life mainly due to the fact that wearing preferentially occurs along surfaces formed by the internal structure of the tooth. It is shown that shape, internal structure, positioning and material characteristics concertedly function in minimizing the rate at which the teeth wear down and in maintaining optimal cutting behaviour. Implementation of these self-sharpening characteristics into industrial cutting devices is discussed. q 2000 Elsevier Science S.A. All rights reserved.
... 88 In mature chiton teeth, aside from elemental and phase disparities, there exist differences in volume and mineral architecture between the leading [the tooth area that interacts with the ingesta; 108,109 This results in a harder and stiffer leading edge and a softer, more flexible trailing edge, which mitigates abrasion during interactions with ingesta surfaces. 55,85,86,88 The disparities in nanocrystal distribution appear rooted in the orientation and density of chitin fibers, where each fiber serves as a mineral nucleating site. Fiber density is higher in the leading edge, yielding more but smaller crystals compared to the trailing edge. ...
... These bundles run perpendicular or parallel to the leading edge, perpendicular to the trailing edge, and bend gradually around the underlying tooth core composed of apatite. [84][85][86]88 Consequently, the chiton tooth is layered with a softer inner core followed by a harder outer magnetite shell, facilitating crack deflection at the core-shell interface. 56 In Patellogastropoda [ Fig. 7(b)], akin to chitons, fiber orientation appears to dictate the arrangement of the goethite crystals, 87,110,111 formed during ontogeny, while interfiber spacing controls crystal thickness. ...
... 84 Fibers and crystals are eventually oriented parallel or perpendicular to the leading surface and perpendicular to the trailing edge in mature teeth; centrally, fibers intersect, reinforcing the entire structure. 86 This, coupled with the overall mineral content, particularly silica, results in a harder leading edge, contributing to self-sharpening effects, general reinforcement, and high resistance to crack initiation and propagation. 58,86,98 Radular teeth in most molluscan species are less mineralized. ...
The Mollusca comprises a diverse range of organisms, with the class Gastropoda alone boasting approximately 80 000 extant species. Their adaptability across various habitats is facilitated by the evolution of the radula, a key structure for food acquisition. The radula's composition and mechanical properties, including its chitinous membrane, teeth, and supporting structures, enable efficient food gathering and processing. Through adaptive tooth morphology and composition, an interplay between radular components is facilitated, which results in collective effects to withstand forces encountered during feeding and reduce structural failure, with the broad range of variations reflecting ecological niches. Furthermore, teeth consist of composite materials with sometimes high contents of iron, calcium, or silicon to reduce wear. During interaction with the food, the radula performs complex three-dimensional motions, challenging to document. Here, we provide a review on the morphology, the mechanical properties, the composition, and various other parameters that contribute to radular performance. Due to, e.g., the smallness of these structures, there are, however, limitations to radular research. However, numerical simulations and physical models tested on substrates offer avenues for further understanding radular function and performance during feeding. These studies not only advance our knowledge of molluscan biology and ecology but also provide inspirations for biomimetic design and further advances in materials engineering.
Published under an exclusive license by the AVS. https://doi.org/10.1116/6.0003672
... Previous studies have used multiple approaches to reveal the performance or functionality of each individual tooth: Feeding tracks were documented and related to radular SEM images (Ankel, 1936(Ankel, , 1938Eigenbrodt, 1941;Hickman & Morris, 1985;Janssen & Triebskorn, 1987;Mackenstedt & Märkel, 2001); the radular motion or feeding action was observed through glass surfaces (Ankel, 1938;Eigenbrodt, 1941;Hawkins et al., 1989;Krings, Faust, et al., 2019;Krings, Neumann, et al., 2021;Scheel et al., 2020;Wägele, 1983); the tooth wear after interaction with abrasive ingesta (e.g., sandpapers of different roughness) was documented to reveal contact areas Krings, Hempel, et al., 2021); physical radular models were constructed (Krings, Karabacak, & Gorb, 2021;Mangan et al., 2005); numerical simulations were computed to study the stress and strain distribution in different tooth types (Krings, Marcé-Nogué, et al., 2020;Krings, Marcé-Nogué, & Gorb, 2021;Miura et al., 2019;van der Wal et al., 1999); and the biomechanical behaviors of the teeth were tested in breaking experiments (Krings, Brütt, & Gorb, 2022a;Krings, Kovalev, & Gorb, 2021a. ...
... limpets, or other gastropod taxa (e.g., the paludomid Lavigeria grandis), the radula transfers high forces to loosen food particles (e.g., algae or biofilms) from solid surfaces (e.g., rocks) by scratching action. Here, each tooth shows pronounced gradients in mechanical properties, with the cusp being the hardest and stiffest region, followed by the stylus, and finally by the base that is the softest and most flexible region Herrera et al., 2015;Krings, Brütt, & Gorb, 2022a;Krings, Matsumura, et al., 2022;Lu & Barber, 2012;Pohl et al., 2020;van der Wal et al., 1999;Weaver et al., 2010). Additionally, some teeth within each row can be harder and stiffer. ...
... Even though the radula is constantly renewed by secretion in the posterior radular region (the radular sac) by overlain and underlain epithelia (Mackenstedt & Märkel, 1987Runham, 1963;Runham & Isarankura, 1966;Vortsepneva et al., 2021;Vortsepneva, Herbert, & Kantor, 2022;Vortsepneva, Mikhlina, & Kantor, 2022), additional mechanisms for wear reduction seem to be present. These mechanisms are well investigated in Polyplacophora and Patellogastropoda; here, very high proportions of Fe and Si are incorporated into the tooth's leading edge (i.e., the surface of the tooth that interacts directly with the ingesta; the posterior surface of the tooth facing towards the radular sac) (e.g., Barber et al., 2015;Han et al., 2011;Lu & Barber, 2012;Saunders et al., 2011;Shaw et al., 2009aShaw et al., , 2009bShaw et al., , 2010van der Wal et al., 1999;Wang et al., 2014;Wealthall et al., 2005;Weaver et al., 2010). We previously identified a similar mechanism, in which high proportions of Ca or Si were detected on the leading edges in teeth of the nudibranch gastropods Doris pseudoargus and Felimare picta, which prey on Porifera, and in the central and lateral teeth of the paludomid L. grandis (Krings et al., 2023;Krings, Brütt, & Gorb, 2022b, 2022c. ...
The radula is the ingesta-gathering structure in Mollusca. As interface, it has to perform various tasks without functional deterioration caused by wear. Wear prevention is well investigated in mollusks that forage on rocks and that generate high punctual pressure with their hard teeth, which contain high inorganic contents at their tips. In mollusks that forage on softer substrate, such as sand surfaces, and have relatively soft teeth, wear prevention has not been a focus of study before. Here, we studied the teeth of Limnotrochus thomsoni, which are used for raking algae from sand. For comparison, we investigated the soft outer teeth of Lavigeria grandis, which are used in gathering particles after the ingesta is loosed from the rock surface. SEM revealed scratches on all surfaces of the teeth and suggests that every tooth side interacts with abrasive particles during foraging. Analysis of stomach content revealed that sand particles of 10–20 μm diameter are ingested. By EDX/EDS, we studied the composition of the teeth and determined that high proportions of Ca are present on all surfaces, which could be an adaptation to reduce abrasion. Finally, we here present evidence for the existence of a canal within the teeth, which could potentially serve as delivery pathway of minerals during tooth maturation and has not been previously detected in Gastropoda.
... 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 (e.g., Herrera et al., 2015;Krings et al., 2022aKrings et al., , 2022dLu & Barber, 2012;van der Wal et al., 1999;Weaver et al., 2010) or to hard structures of the prey (e.g., sponge spiculae) by piercing action (Krings et al., 2023). ...
... 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 Herrera et al., 2015;Krings et al., 2019Krings et al., , 2022cKrings et al., , 2022dKrings et al., , 2023Lu & Barber, 2012;Pohl et al., 2020;van der Wal et al., 1999;Weaver et al., 2010). 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. ...
... 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 from algae growing on stones (e.g., Barber et al., 2015;Han et al., 2011;Krings et al., 2022c;Lu & Barber, 2012;Saunders et al., 2011;Shaw et al., 2009aShaw et al., , 2009bShaw et al., , 2010van der Wal et al., 1999;Wang et al., 2014;Wealthall et al., 2005;Weaver et al., 2010). 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 from rocks and Nudibranchia foraging on Porifera) as well. ...
The molluscan feeding structure is the radula, a chitinous membrane with teeth, which are highly adapted to the food and the substrate to which the food is attached. In Polyplacophora and Patellogastropoda, the handling of hard ingesta can be facilitated by high content of chemical compounds containing Fe or Si in the tooth cusps. Other taxa, however, possess teeth that are less mineralized, even though animals have to avoid structural failure or high wear during feeding as well. Here, we investigated the gastropod Gastropteron rubrum , feeding on hard Foraminifera, diatoms and Porifera. Tooth morphologies and wear were documented by scanning electron microscopy and their mechanical properties were tested by nanoindentation. We determined that gradients of hard‐ and stiffness run along each tooth, decreasing from cusp to basis. We also found that inner lateral teeth were harder and stiffer than the outer ones. These findings allowed us to propose hypotheses about the radula‐ingesta interaction. In search for the origins of the gradients, teeth were visualized using confocal laser scanning microscopy, to determine the degree of tanning, and analyzed with energy‐dispersive X‐ray spectroscopy, to test the elemental composition. We found that the mechanical gradients did not have their origins in the elemental content, as the teeth did not contain high proportions of metals or other minerals. This indicates that their origin might be the degree of tanning. However, in the tooth surfaces that interact with the ingesta high Si and Ca contents were determined, which is likely an adaptation to reduce wear.
... Besides different local degrees of tanning, which result in different local mechanical properties [52], the matrix can vary in its fibre orientation, density or arrangement [45,46,[66][67][68][69][70][71][72][73][74]. The tooth surface can consist of a layer without larger fibres, whereas the underlying layer rather consists of fibres oriented perpendicularly to the tooth surface, probably absorbing shocks during interaction with the ingesta [60,[74][75][76][77][78][79] and transmitting stresses to the radular membrane [80]. (3) Additionally, in some taxa such as Polyplacophora or Patellogastropoda, high proportions of inorganics such as iron, silicon and calcium are incorporated in the tooth cusps as mechanical adaptations to the foraging on harder substrates (for reviews, see [81][82][83]). ...
... Especially, the interacting surfaces of teeth, the leading edges, can be highly adapted to the interaction with the ingesta. In addition to the fibre architecture, a high proportion of inorganic material results in a harder and stiffer leading edge, reducing wear and structural failure, in contrast with the softer and more flexible trailing edge and the tooth core [44,76,77,79,[84][85][86][87][88][89][90][91][92]. As a consequence, teeth can be layered with a softer inner core, followed by a thick harder outer layer, which reduces crack formation at the core-shell interface [46,75,76]. ...
... In addition to the fibre architecture, a high proportion of inorganic material results in a harder and stiffer leading edge, reducing wear and structural failure, in contrast with the softer and more flexible trailing edge and the tooth core [44,76,77,79,[84][85][86][87][88][89][90][91][92]. As a consequence, teeth can be layered with a softer inner core, followed by a thick harder outer layer, which reduces crack formation at the core-shell interface [46,75,76]. Leading and trailing edges were well investigated in chitons and limpets, but for the majority of gastropods there is a lack of knowledge, as only one non-limpet species was studied previously (Lavigeria grandis, Paludomidae, Caenogastropoda) [74]. ...
Molluscs forage with their radula, a chitinous membrane with teeth. Adaptations to hard or abrasive ingesta were well studied in Polyplacophora and Patellogastropoda, but for other taxa there are large gaps in knowledge. Here, we investigated the nudibranch gastropods Felimare picta and Doris pseudoargus, both of which feed on Porifera. Tooth morphologies were documented by scanning electron microscopy, and mechanical properties were tested by nanoindentation. We found that these parameters are rather similar in both species, indicating that teeth are similar in their function. To study the composition, teeth were visualized using confocal laser scanning microscopy (CLSM), to determine the degree of tanning, and analysed with energy-dispersive X-ray spectroscopy, to test the elemental composition. The emitted autofluorescence signal and the inorganic content differed between the species. This was especially prominent when studying the inner and outer tooth surfaces (leading and trailing edges). In F. picta, we detected high proportions of Si, whereas teeth of D. pseudoargus contained high amounts of Ca, which influenced the autofluorescence signal in CLSM. Employing nanoin-dentation, we determined high Young's modulus and hardness values for the leading edges of teeth, which relate to the Si and Ca content. This highlights that teeth with a similar morphology and mechanical properties can be mechanically enhanced via different chemical pathways in Nudibranchia.
... 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., 2019Krings et al., , 2022cKrings et al., , 2022dKrings et al., , 2023Pohl 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. ...
... 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., 2009aShaw et al., , 2009bShaw et al., , 2010Weaver 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. ...
... Wear reducing mechanisms are well-investigated in Polyplacophora and Patellogastropoda. Here, high proportion of Fe and Si are incorporated into a thick leading edge (surface layer), which is hard and protected against wear (Kirschvink & Lowenstam, 1979;Kim et al., 1989;Lowenstam & Weiner, 1989;van der Wal, 1989;van der Wal et al., 1999;Brooker et al., 2003;Lee et al., 2003aLee et al., , 2003bSaunders et al., 2009Saunders et al., , 2011Weaver et al., 2010;Wang et al., 2013;Kisailus & Nemoto, 2018;Krings et al., 2022c). Compared to the harder outer edge, the teeth possess a softer inner structure, which reduces crack formation (van der Wal, 1989;van der Wal et al., 1999;Grunenfelder et al., 2014). ...
The molluscan feeding structure is the radula, a chitinous membrane with teeth, which are highly adapted to the food and the substrate. In Polyplacophora and Patellogastropoda, the handling of hard ingesta can be facilitated by high content of chemical compounds containing Fe or Si in the tooth cusps. Other taxa, however, possess teeth that are less mineralized, even though animals have to avoid structural failure or high wear during feeding as well. Here, we investigated the gastropod Gastropteron rubrum , feeding on hard Foraminifera, diatoms and Porifera. Tooth morphologies and wear were documented by scanning electron microscopy and their mechanical properties were tested by nanoindentation. We determined, that gradients of hard- and stiffness run along each tooth, decreasing from cusp to basis. We also found, that inner lateral teeth are harder and stiffer than the outer ones. These findings allowed us to propose hypotheses about the radula-ingesta interaction. In search for the origins of the gradients, teeth were visualized using confocal laser scanning microscopy, to determine the degree of tanning, and analyzed with energy-dispersive X-ray spectroscopy, to test the elemental composition. We found that the mechanical gradients probably have their origin in the degree of tanning, as the teeth did not contain high proportions of metals or other minerals. However, in the tooth surfaces, which interact with the ingesta, high Si and Ca content was determined, which is likely an adaptation to reduce wear.
... The dominant lateral teeth of these taxa, used for loosening algae from rocky feeding substrates, were very well studied in the last decades due to their immense hardness and stiffness [for throughout reviews see [41][42][43]. These mechanical properties are based on substantial proportions of iron-based incorporations, which increase the cusps' wear-resistance [17,20,[44][45][46][47][48][49], and at least one non-iron element incorporated in teeth (e.g. silicon, calcium), probably serving as mechanical reinforcement [42]. ...
... This is in congruence with our results from the breaking stress experiments in Lepidochitona and paludomid gastropods [25,27], where we observed that the wet membrane is flexible enough to enable the bending of embedded teeth and additionally contributes to stress distribution. The dominant lateral tooth cusps possess caps of exceptional hardness, reducing wear and contributing to a self-sharpening effect [17,19,47,105,107; see also 103 for limpets]. This, together with their high ability to resist forces (documented here) and with the previously documented foraging behaviour and observed rotating interaction of the dominant lateral teeth with the ingesta surface [1,30,109], depicts that these teeth loosen the food from the hard surface and transport them towards the mouth [43,97]. ...
... It was previously reported that due to the specific shape of the cusp and the gradients in hardness and Young's modulus across the tooth, tensile stress is concentrated on the leading edge and reduced in the trailing edge, reducing the ability of the tooth to bend and thus reduce the failure of the sharp tip of the tooth [19,47]. It was also reported that the stylus enables the sweeping action during feeding [95,97], orients the tooth to the ingesta [47], but also transfers force from the basis to the tooth cusp [98] leading to the reduction of structural failure [97]. ...
Background: The radula, a chitinous membrane with embedded teeth, is one important molluscan autapomorphy. In some taxa (Polyplacophora and Patellogastropoda) one tooth type (the dominant lateral tooth) was studied intensively in the last decades with regard to its mechanical properties, chemical and structural composition, and the relationship between these parameters. As the dominant lateral tooth is probably one of the best studied biological materials, it is surprising, that data on elements and mechanical properties of the other tooth types, present on a chiton radula, is lacking.
Results: We provide data on the elemental distribution and mechanical properties (hardness and elasticity, i.e. Young’s modulus) of all teeth from the Polyplacophora Lepidochitona cinerea (Linnaeus, 1767) [Chitonidae: Ischnochitonidae]. The ontogeny of elements, studied by energy-dispersive X-ray spectroscopy, and of the mechanical properties, determined by nanoindentation, was analysed in every individual tooth type. Additionally, we performed breaking stress experiments with teeth under dry and wet condition, highlighting the high influence of the water content on the mechanical behaviour of the radula. We thereby could determine the forces and stresses, teeth can resist, which were previously not studied in representatives of Polyplacophora. Overall, we were able to relate the mineral (iron, calcium) content with the mechanical parameters (hardness and Young’s modulus) and the breaking force and stress in every tooth type. This led to a better understanding of the relationship between structure, material, and function in radular teeth. Further, we aimed at determining the role of calcium for the mechanical behaviour of the teeth: we decalcified radulae by ethylene diamine tetra acetic acid and performed afterwards elemental analyses, breaking stress experiments, and nanoindentation. Among other things, we detected that wet and decalcified radular teeth could resist highest forces, since teeth have a higher range of bending motion leading to a higher capability of teeth to gain mechanical support from the adjacent tooth row. This indicates, that the tooth material is the result of a compromise between failure reduction and the ability to transfer forces onto the ingesta.
Conclusion: We present novel data on the elemental composition, mechanical properties, and the mechanical behaviour of chiton teeth, which allows conclusions about tooth function. We could also relate the parameters mentioned, which contributes to our understanding on the origins of mechanical property gradients and the processes reducing structural failure in radular teeth. Additionally, we add more evidence, that the elemental composition of radular is probably species-specific and could be used as taxonomic character.
... The tight interaction of teeth with the ingesta leads to some tooth wear (e.g. [7][8][9][10][11][12], but the radula is constantly secreted and maturated by overlain epithelia in its posterior parts, the radular sack and formation zone Model system African Paludomidae. The Paludomidae from Lake Tanganyika and surrounding water bodies are representatives of a species flock, that is potentially the result of an adaptive radiation accompanied by trophic specialisation (for hypotheses on paludomid evolution see e.g. ...
... For radular teeth, the importance of the heterogeneous distribution of material properties was previously also determined in docoglossan teeth of Patella and Polyplacophora; here 7 detected that the tooth's part, interacting in the ingesta, is harder and stiffer, whereas the underlain parts are softer and more flexible (see also 58 for the flexibility of the stylus). The co-appearance of harder and softer layers probably leads to a reduction of abrasion in the radular cusps 7,46 as observed in other structures as well (e.g. 54,111 ). ...
... When all models are loaded with the nominal force (forces are corrected for the radular size) the radula of Bridouxia grandidieriana possess the largest area with high concentrations of stress and strain, followed by Cleopatra johnstoni, Spekia zonata, and finally Lavigeria grandis(Figs. 5,6,7,8). With decreasing load in each species, stress and strain concentrations are reduced. ...
The radula, a chitinous membrane with embedded tooth rows, is the molluscan autapomorphy for feeding. The morphologies, arrangements and mechanical properties of teeth can vary between taxa, which is usually interpreted as adaptation to food. In previous studies, we proposed about trophic and other functional specialisations in taenioglossan radulae from species of African paludomid gastropods. These were based on the analysis of shape, material properties, force‑resistance, and the mechanical behaviour of teeth, when interacting with an obstacle. The latter was previously simulated for one species (Spekia zonata) by the finite‑element‑analysis (FEA) and, for more species, observed in experiments. In the here presented work we test the previous hypotheses by applying the FEA on 3D modelled radulae, with incorporated material properties, from three additional paludomid species. These species forage either on algae attached to rocks (Lavigeria grandis), covering sand (Cleopatra johnstoni), or attached to plant surface and covering sand (Bridouxia grandidieriana). Since the analysed radulae vary greatly in their general size (e.g. width) and size of teeth between species, we additionally aimed at relating the simulated stress and strain distributions with the tooth sizes by altering the force/volume. For this purpose, we also included S. zonata again in the present study. Our FEA results show that smaller radulae are more affected by stress and strain than larger ones, when each tooth is loaded with the same force. However, the results are not fully in congruence with results from the previous breaking stress experiments, indicating that besides the parameter size, more mechanisms leading to reduced stress/strain must be present in radulae.
... Fe, can be incorporated in the chitin matrix probably leading to a greater wear resistance [e.g. [30][31][32][33][34][35][36][37][38][39][40][41][42][43]. The different proportions of the found chemical constituents are thought to cause the measured mechanical properties of the previously studied Patellogastropoda and Polyplacophora species [e.g. ...
... FEA was also applied in studying food processing structures as beaks of Darwin's finches providing engineering evidence for trophic specialization [89] and is a useful approach to provide a comparative perspective on radular teeth mechanics. In Malacological objects FEA had already been used for understanding the functionality of Patella , Polyplacophora [37] and Euhadra [90] radular teeth. Van der Wal et al. [37] designed a FEA study including considerations on the material gradients and mechanical properties of teeth. ...
... In Malacological objects FEA had already been used for understanding the functionality of Patella , Polyplacophora [37] and Euhadra [90] radular teeth. Van der Wal et al. [37] designed a FEA study including considerations on the material gradients and mechanical properties of teeth. However, their study lacks the exact 3D morphology, which at that time could not be included in FEA due to lacking computing capacity. ...
Molluscs are a highly successful group of invertebrates characterised by a specialised feeding organ called the radula. The diversity of this structure is associated with distinct feeding strategies and ecological niches. However, the precise function of the radula (each tooth type and their arrangement) remains poorly understood. Here for the first time, we use a quantitative approach, Finite-Element-Analysis (FEA), to test hypotheses regarding the function of particular taenioglossan tooth types. Taenioglossan radulae are of special interest, because they are comprised of multiple teeth that are regionally distinct in their morphology. For this study we choose the freshwater gastropod species Spekia zonata, endemic to Lake Tanganyika, inhabiting and feeding on algae attached to rocks. As a member of the African paludomid species flock, the enigmatic origin and evolutionary relationships of this species has received much attention. Its chitinous radula comprises several tooth types with distinctly different shapes. We characterise the tooth's position, material properties and attachment to the radular membrane and use this data to evaluate 18 possible FEA scenarios differing in the above parameters. Our estimations of stress and strain indicate different functional loads for different teeth. We posit that the central and lateral teeth are best suitable for scratching substrate loosening ingesta, whereas the marginals are best suited for gathering food particles. Our successful approach and workflow are readily applicable to other mollusc species.
... Despite the constant renewal of the radula, certain wear coping mechanisms aim at reducing wear and structural failure. In members of Polyplacophora (Weaver et al. 2010;Krings, Brütt, and Gorb 2022d;Wealthall et al. 2005;Shaw et al. 2009aShaw et al. , 2009bSaunders et al. 2011;Han et al. 2011;Wang et al. 2014), Cephalopoda (Hackethal et al. 2024), and members of the gastropod groups Patellogastropoda (e.g., Lu and Barber 2012;Barber, Lu, and Pugno 2015;van der Wal, Giesen, and Videler 1999;Shaw et al. 2010), Paludomidae (Krings, Brütt, and Gorb 2022c;Krings and Gorb 2023a), Cephalaspidea , and some Nudibranchia , this involves the incorporation of elevated levels of iron (Fe), calcium (Ca), or silicon (Si) into the superficial regions of teeth that interact with ingesta. This results in harder tooth cusps capable of withstanding hard and abrasive ingesta, like Porifera spiculae, crustacean carapaces, Foraminifera, or algae attached to stone surfaces. ...
... with the ingesta, and almost completely fill the internal tooth structure (see, e.g., Weaver et al. 2010;Lu and Barber 2012;Barber, Lu, and Pugno 2015;van der Wal, Giesen, and Videler 1999;Wealthall et al. 2005;Shaw et al. 2009aShaw et al. , 2009bShaw et al. , 2010Saunders et al. 2011;Han et al. 2011;Wang et al. 2014;Kirschvink and Lowenstam 1979). The teeth of the cephalopod L. vulgaris, the nudibranch gastropods D. pseudoargus and F. picta, the heterobranch gastropod G. rubrum, and some paludomids, in contrast, lack these minerals in their internal structures. ...
Nudibranchs, with their mesmerizing diversity and ecological significance, play crucial roles in marine ecosystems. Central to their feeding prowess is the radula, a chitinous structure with diverse morphologies adapted to prey preferences and feeding strategies. This study focuses on elucidating wear coping mechanisms in radular teeth of carnivorous molluscs, employing Dendronotus lacteus (Dendronotidae) and Flabellina affinis (Flabellinidae) as model species. Both species forage on hydrozoans. Through scanning electron microscopy, confocal laser scanning microscopy, nanoindentation, and energy-dispersive X-ray spectroscopy, the biomechanical and compositional properties of their teeth were analyzed. Notably, tooth coatings, composed of calcium (Ca) or silicon (Si) and high hardness and stiffness compared to the internal tooth structure, with varying mineral contents across tooth regions and ontogenetic zones, were found. The presence of the hard and stiff tooth coatings highlight their role in enhancing wear resistance. The heterogeneities in the autofluorescence patterns related to the distribution of Ca and Si of the coatings. Overall, this study provides into the biomechanical adaptations of nudibranch radular teeth, shedding light on the intricate interplay between tooth structure, elemental composition, and ecological function in marine molluscs.
... iron oxides and silica in Polyplacophora and Patellogastropoda; e.g. [4,[8][9][10][11][12][13][14][15][16][17][18]), in the degree of tanning (e.g. some paludomid, nudibranch or heterobranch gastropods; see [22,23,37]), or in the amount of cross-linkers between the chitin fibres (e.g. ...
... Wear prevention is well documented for the teeth of Polyplacophora and Patellogastropoda, where very high proportions of Fe and Si are incorporated into the tooth's thick leading edge (i.e. the surface of the tooth that interacts directly with the ingesta) (e.g. [4,[8][9][10][11][12][13][14][16][17][18]168,169]). In the almost unmineralized teeth of the nudibranch gastropods Doris pseudoargus and Felimare picta foraging on Porifera, the cephalaspid gastropod Gastropteron rubrum, and some paludomid gastropods, we previously documented a similar mechanism. ...
Radular teeth have to cope with wear, when interacting with ingesta. In some molluscan taxa, wear-coping mechanisms, related to the incorporation of high contents of iron or silica, have been previously determined. For most species, particularly for those which possess radulae without such incorporations, wear-coping mechanisms are understudied. In the present study, we documented and characterized the wear on radular teeth in the model species Loligo vulgaris (Cephalopoda). By applying a range of methods, the elementary composition and mechanical properties of the teeth were described, to gain insight into mechanisms for coping with abrasion. It was found that the tooth regions that are prone to wear are harder and stiffer. Additionally, the surfaces interacting with the ingesta possessed a thin coating with high contents of silicon, probably reducing abrasion. The here presented data may serve as an example of systematic study of radular wear, in order to understand the relationship between the structure of radular teeth and their properties.
... The chitin fibres of L. grandis teeth were oriented perpendicular to the leading surface, similar to the situation in limpets and chitons [47,64,65]. The fibre orientation probably contributes to the wear-and fracture-resistance, since the local properties and performance of biological materials, which are composed of anisotropic structural units, highly depend on the orientation of these units (fibres, tubules, crystals etc. interior of the structure and become tilted to the exterior, leading to higher stiffness towards the surface and higher fracture resistance with depth [99]. ...
... The fibre orientation probably contributes to the wear-and fracture-resistance, since the local properties and performance of biological materials, which are composed of anisotropic structural units, highly depend on the orientation of these units (fibres, tubules, crystals etc. interior of the structure and become tilted to the exterior, leading to higher stiffness towards the surface and higher fracture resistance with depth [99]. Additionally, some fibres in L. grandis (e.g. on the lateral side of the stylus of the marginal and lateral teeth) run perpendicular to the radular membrane and thus cross the parallel-running fibres, which probably, similar to the situation in limpets and chitons, reduces crack propagation [47,64,65]. ...
Most molluscan taxa forage with their radula, a chitinous membrane with embedded teeth. The teeth are the actual interfaces between the animal and its ingesta and serve as load-transmitting regions. During foraging, these structures have to withstand high stresses without structural failure and without a high degree of wear. Mechanisms contributing to this failure- and wear-resistance were well studied in the heavily mineralized teeth of Polyplacophora and Patellogastropoda, but for the rather chitinous teeth of non-limpet snails, we are confronted with a large gap in data. The work presented here on the paludomid gastropod Lavigeria grandis aims to shed some light on radular tooth composition and its contribution to failure- and wear-prevention in this type of radula. The teeth were fractured and the micro-cracks studied in detail by scanning electron microscopy, revealing layers within the teeth. Two layers of distinct fibre densities and orientations were detected, covered by a thin layer containing high proportions of calcium and silicon, as determined by elemental dispersive X-ray spectroscopy. Our results clearly demonstrate the presence of failure- and wear-prevention mechanisms in snail radulae without the involvement of heavy mineralization—rendering this an example of a highly functional biological lightweight structure.
This article is part of the theme issue 'Nanocracks in nature and industry'.
... Natural wear has been documented in various molluscan species 6,8,10,24,46,[61][62][63][64][65][66][67] , but wear-causing agents have not been reported in these publications. Comparing results from previous studies with the ones obtained here depict that the natural wear in Polyplacophora and Patellogastropoda 24 is heavier than the wear observed in the radulae from our control group. ...
... After the cusps break off, e.g. in lateral tooth II, gastropods seem to forage with the remaining stylus, until this structure is also worn down [see also 46]. We did not find any signs of a self-sharpening effect as previously described for chitons, limpets, and echinoderms 10,24,65,77,78 . However, obviously damaged teeth can, to a certain extent, still maintain their function. ...
The radula is the food gathering and processing structure and one important autapomorphy of the Mollusca. It is composed of a chitinous membrane with small, embedded teeth representing the
interface between the organism and its ingesta. In the past, various approaches aimed at connecting the tooth morphologies, which can be highly distinct even within single radulae, to their functionality.
However, conclusions from the literature were mainly drawn from analyzing mounted radulae, even though the configuration of the radula during foraging is not necessarily the same as in mounted
specimens. Thus, the truly interacting radular parts and teeth, including 3D architecture of this complex structure during foraging were not previously determined. Here we present an experimental approach on individuals of Vittina turrita (Neritidae, Gastropoda), which were fed with algae paste attached to different sandpaper types. By comparing these radulae to radulae from control group, sandpaper-induced tooth wear patterns were identified and both area and volume loss could be quantified. In addition to the exact contact area of each tooth, conclusions about the 3D position of teeth and radular bending during feeding motion could be drawn. Furthermore, hypotheses about specific tooth functions could be put forward. These feeding experiments under controlled conditions were introduced for stylommatophoran gastropods with isodont radulae and are now applied to heterodont and complex radulae, which may provide a good basis for future studies on radula functional morphology.
... This interaction naturally leads to tooth wear (e.g. [6][7][8][9][10]) and probably also structural failure, but through a continuous growth from posterior to anterior the radular membrane and its teeth are always replaced (e.g. [11][12][13][14][15]). ...
... Approaches aiming at relating the gastropod's feeding ecology with the function of its radular teeth (e.g. scratching, loosening food items, collecting and gathering particles) had been undertaken [7,[21][22][23][24][25][26][27][28][29], but in most previous studies hypotheses are primarily based on the consideration of the tooth shape and only few include the mechanical properties (usually elasticity modulus = Young's modulus, or hardness) of teeth. Additionally, the individual components of the radula interact during foraging [30,31]. ...
One molluscan autapomorphy is the radula, the organ used for feeding. Here, for the first time, the performance and failure of taenioglossan radular teeth were tested in a biomechanical experiment which in turn allowed building hypotheses about tooth functionalities. Shear load was applied to tooth cusps with a force transducer until structural failure occurred, the broken area was measured, and finally breaking stress was calculated. These experiments were carried out under dry and wet conditions. Our results show that certain tooth types can resist higher stresses and are rather specialised to loosen food items from a surface whereas other teeth can only gather food particles. The experiments additionally illustrate the high influence of the water content on the resulting breaking stress. When wet teeth were tested, their ductility and ability to avoid being fractured by an obstacle increased. Their flexibility also allowed them support from teeth of adjacent tooth rows, which made the whole system less prone to failure. Our results were compared with the previous data on the mechanical properties and feeding simulations. This study provides a keystone for further comparative studies aiming at connecting diversity of radulae with their possible adaptations to the ingesta.
... In turn, this aid in better understanding performance of teeth, and their ability to resist stresses. In addition, the precise areas of contact are needed for simulating biomechanical behaviour in numerical approaches (Finite-Element-Analyses, FEA), since the areas act as load transmitting regions [for FEA of radular teeth see [31][32][33]. ...
... 2,20] used while feeding, which is congruent to our results. However, the quantity of transversal tooth rows showing signs of wear varies between 4 and 26 anterior rows according to the literature data (for Patellogastropoda and Polyplacophora: [31]: 8-11 rows; [6]: 4 rows in chitons, 8 rows in limpets; Vetigastropoda: [3]: 6-9 rows; Caenogastropoda: [48]: 14-32 rows; Heterobranchia: [1]: 26 rows, [70]: <15 rows). As the amount of worn tooth rows in our study clearly correlates with the target surface roughness, we expect similar contact mechanics and wear mechanisms for other molluscan taxa. ...
Determining a precise contact area between one surface and another surface is essential for understanding tribo-logical tool performance, since this area contributes to the force transmission. Radular teeth are part of the complex molluscan feeding apparatus acting on the ingesta by transmitting muscle-driven forces, in some cases working as a puncturing tool. Various approaches aimed at identifying the contact areas and cutting edges of radular teeth to understand the relationship between both shape and position of teeth and the function. However, most previous studies rely on feeding tracks which are difficult to interpret. To determine load transmitting regions, we here present an easy experimental setup involving sandpaper that can be applied to a variety of molluscan species. Stylommatophoran gastropods were fed with food paste attached to sandpapers of different roughness for 1 month: subsequently, the radular tooth wear was analysed qualitatively. These feeding experiments under controlled conditions were performed for molluscan radula for the first time revealing distinct sandpaper-induced facets. Comparisons of the tooth material loss led to the determination of the contact areas and the amount of teeth involved in the feeding process, both directly related with the surface roughness. Additionally, the direction of force during feeding was reconstructed. The analyses of wear patterns resulting from the impact of teeth on the sandpaper grains contribute to our knowledge about the underlying mechanisms preventing structural failure in radulae. These mechanisms are based on the biomechanical behaviour of the radular supporting structures.
... Natural wear has been documented in various molluscan species [6,8,10,24,44,[59][60][61][62][63][64][65], but wear-causing agents have not been reported in these publications. ...
... After the tooth cusps break off, as in the lateral tooth II, the gastropods seem to forage with the remaining stylus, until this structure is also worn down [see also 44]. We did not nd any signs of a self-sharpening effect as previously described for chitons, limpets, and echinoderms [10,24,63,[75][76]. However, obviously damaged teeth can, to a certain extent, still maintain their function. ...
The radula is the food gathering and processing structure and one important autapomorphy of the Mollusca. It is composed of a chitinous membrane with small, embedded teeth representing the interface between the organism and its ingesta. In the past, various approaches aimed at connecting the tooth morphologies, which can be highly distinct even within single radulae, to their functionality. However, conclusions from the literature were mainly drawn from analyzing mounted radulae, even though the configuration of the radula during foraging is not necessarily the same as in mounted specimens. Thus, true interacting radular parts, which are essential for determining tooth’s functionality, including 3D architecture of this complex feeding structure were not previously determined. In the here presented experimental approach individuals of Vittina turrita (Neritidae, Gastropoda) were fed with algae paste attached to different sandpaper types. By comparison with radulae from control group, sandpaper-induced tooth wear patterns were identified and both area and volume loss were quantified. In addition to the exact contact area of each tooth, conclusions about the 3D position of teeth and radular bending during feeding motion could be drawn. Furthermore, hypotheses about specific tooth functions could be put forward. These feeding experiments under controlled conditions were introduced on stylommatophoran gastropods with isodont radulae and are here applied to heterodont and complex radulae, which may provide a good basis for future studies on radula functional morphology.
... The teeth of chitons and limpet have been used as a unique model for the systematic study of iron mineralization processes, not only due to the good mechanical properties of mineralization products (van der Wal et al., 2000;Grunenfelder et al., 2014;Barber et al., 2015), but also due to the different stages of mineral development that can be observed in a single radula structure (Sone et al., 2005;Sone et al., 2007;Ruggeberg et al., 2010). It has been discovered that the cusps of many species of limpet teeth are constructed of a preformed achitin matrix filled with goethite(a-FeOOH) and amorphous hydrated silica (SiO 2 ·nH 2 O) (Grime et al., 1985;Burford et al., 1986;Mann et al., 1986;Wal, 1989;Lu et al., 1995;Sone et al., 2007). ...
Limpets are a class of marine mollusks that use mineralized teeth, one of the hardest and strongest biological materials, to feed on algae on rocks. By combining proteomics and RNA-seq analysis of limpet radula, we identified a novel chitin-binding protein (CtCBP-1) that may play a regulatory role in radula mineralization of Cellana toreuma. In this study, the full-length cDNA of CtCBP-1 gene was cloned for the first time, and the protein was successfully expressed in vitro. In vitro experiments demonstrated that CtCBP-1 binds well to both goethite and chitin, which are key components of the cusp. We studied the function of CtCBP-1 on goethite crystallization in vitro, revealing that it changed the morphology of goethite crystals. We also used fluorescence higher resolution imaging to map the binding of CtCBP-1 in radula and found that the distribution of CtCBP-1 on radula was specific, which consistent with the SEM results finding tightly aligned goethite. In this study, a novel protein CtCBP-1, which regulates the distinctive biomineralization process of limpet teeth, is identified for the first time. This protein’s identification may inform biomimetic techniques for creating hard materials that can withstand ambient temperature.
... Scale bars: a 10 mm; b 125 µm their absence to softer and more flexible tooth styli and bases (e.g. Runham et al. 1969;Vincent 1980;van der Wal et al. 1999;Weaver et al. 2010;Grunenfelder et al. 2014;Barber et al. 2015;Krings et al. 2022c; for throughout reviews, see Brooker and Shaw 2012;Faivre and Ukmar-Godec 2015;Joester and Brooker 2016). In addition, the degree of cross-linking seems to contribute to the functional gradients in the mechanical properties in these taxa (Runham 1963;Ukmar-Godec et al. 2017). ...
The radula, a chitinous membrane spiked with teeth, is the molluscan autapomorphy for the gathering and processing of food. The teeth, as actual interfaces between the organism and the ingesta, act as load transmitting regions and have to withstand high stresses during foraging-without structural failure or high degrees of wear. Mechanisms contributing to this were studied previously in paludomid gastropods from Lake Tanganyika. For some species, gradients in hardness and Young's modulus along the teeth were detected, enabling the bending and relying of teeth onto the next row, distributing the stresses more equally. The here presented study on one of them-Lavigeria grandis-aims at shedding light on the origin of these functional gradients. The mechanical properties were identified by nanoindentation technique and compared to the elemental composition, determined by elemental dispersive X-ray spectroscopy (EDX, EDS). This was done for the complete radular (mature and immature tooth rows), resulting in overall 236 EDX and 700 nanoindentation measurements. Even though teeth showed regional differences in elemental composition, we could not correlate the mechanical gradients with the elemental proportions. By applying confocal laser scanning microscopy (CLSM), we were finally able to relate the mechanical properties with the degree of tanning. CLSM is a common technique used on arthropod cuticle, but was never applied on radular teeth before. In general, we found that nanoindentation and CLSM techniques complement one another, as for example, CLSM is capable of revealing heterogeneities in material or micro-gradients, which leads to a better understanding of the functionalities of biological materials and structures.
... During foraging, the cusps directly interact with the natural ingesta (food, substrate, minerals, everything that is taken in) which results in some tooth wear [e.g. [26][27][28][29][30], but usually not in structural failure of teeth or membrane. Teeth and membrane are replaced constantly by epithelial secretion in the posterior part of the radula [e.g. ...
The molluscan radula, a thin membrane with embedded rows of teeth, is the structure for food processing and gathering. For proper functioning, radular failures must be either avoided or reduced when interacting with the preferred food, as this might be of high significance for the individual fitness. Thus, the analysis of structural failure in radular teeth could be included in studies on trophic specializations. Here, we tested the failure of non-mineralized, chitinous radular teeth from taxa, belonging to an African paludomid species flock from Lake Tanganyika and surrounding river systems. These species are of high interest for evolutionary biologists since they represent a potential result of an adaptive radiation including trophic specialisations to distinct substrates, the food is attached to. In a biomechanical experiment a shear load was applied to tooth cusps with a force transducer connected to a motorized stage until structural failure occurred. Subsequently broken areas were measured and breaking stress was calculated. As the experiments were carried out under dry and wet conditions, the high influence of the water content on the forces, teeth were capable to resist, could be documented. Wet teeth were able to resist higher forces, because of their increased flexibility and the flexibility of the embedding membrane, which enabled them either to slip away or to gain support from adjacent teeth. This mechanism can be understood as collective effect reducing structural failure without the mineralisation with wear-minimizing elements, as described for Polyplacophora and Patellogastropoda. Since the documented mechanical behaviour of radular teeth and the maximal forces, teeth resist, can directly be related to the gastropod ecological niche, both are here identified as an adaptation to preferred feeding substrates.
Statement of significance
: The radula, a chitinous membrane with teeth, is the molluscan feeding structure. Here we add onto existing knowledge about the relationship between tooth's mechanical properties and species’ ecology by determining the tooth failure resistance. Six paludomid species (Gastropoda) of a prominent species flock from Lake Tanganyika, foraging on distinct feeding substrates, were tested. With a force transducer wet and dry teeth were broken, revealing the high influence of water content on mechanical behaviour and force resistance of teeth. Higher forces were needed to break wet radulae due to an increased flexibility of teeth and membrane, which resulted in an interlocking or twisting of teeth. Mechanical behaviour and force resistance were both identified as trophic adaptations to feeding substrate.
... The hardness and elastic modulus (Young's modulus) relates to the ingesta as well e.g. [33,34] . Radular teeth of some molluscan taxa, Polyplacophora and Patellogastropoda, are very hard and stiff, caused by high proportions of incorporated iron, reducing tooth wear when interacting with algae attached to solid sub-strates [ 3 , 34-47 ]. ...
Biological tissues may exhibit graded heterogeneities in structure and mechanical properties that are crucial to their function. One biological structure that shows variation in both structure and function is the molluscan radula: the organ comprises a chitinous membrane with embedded teeth and serves to process and gather food. The tooth morphologies had been well studied in the last decades, but the mechanical properties of the teeth are not known for the vast majority of molluscs. This knowledge gap restricts our understanding of how the radula is able to act effectively on a target surface whilst simultaneously resisting structural failure. Here we employed nanoindentation technique to measure mechanical properties (hardness and Young's modulus) on distinct localities of individual radular teeth from 24 species of African paludomid gastropods. These species have distinct ecological niches as they forage on algae on different feeding substrates. A gradual distribution of measured properties along the teeth was found in species foraging on solid or mixed feeding substrates, but soft substrate feeders exhibit teeth almost homogeneous in their biomechanical properties. The presence or absence of large-scale gradients in these taenioglossan teeth could directly be linked with their specific function and in general with the species ecology, whereas the radular tooth morphologies do not always and fully reflect ecology.
... Persistent polyamorphism in the chiton tooth: From a new biomineral to inks for additive manufacturing tooth head during the feeding stroke ( Fig. 1D and SI Appendix, Fig. S10 A and B) (19). The stylus connects the tooth head to the radula and orients the tooth with respect to the substratum (20). The radula membrane ( Fig. 1D and SI Appendix, Fig. S10C) has lower stiffness to accommodate complex shape changes but at the same time must be strong, tough, and resistant to fatigue to survive the cycling bending and unbending during feeding. ...
Significance
Biomineralization is a highly successful strategy to create functionally graded materials with complex shape. Herein, we demonstrate that the rock-grazing mollusk Cryptochiton stelleri uses two amorphous, yet structurally distinct, phases in neighboring microarchitectural domains to reinforce its dentition. Nano-disperse santabarbaraite, an amorphous iron hydroxyphosphate, is present in the stylus, extending the range over which hardness and stiffness vary by at least a factor of two. Use of ferric phosphates with low iron and high water content may present a stratagem to create strong composites with low density. Indeed, we show that bio-inspired inks based on chitosan and mineral precursors allow three-dimensional printing of tunable composites strengthened by amorphous nanoparticles precipitated in situ.
... During foraging, the cusps directly interact with the natural ingesta (food, substrate, minerals, everything that is taken in) which results in some tooth wear [e.g. [26][27][28][29][30], but usually not in structural failure of teeth or membrane. Teeth and membrane are replaced constantly by epithelial secretion in the posterior part of the radula [e.g. ...
... Ankel, 1938;Eigenbrodt, 1941;Märkel, 1964) and so the teeth and tooth rows are capable of interacting to distribute force and stress (Solem, 1972;Hickman, 1984). The performance and function of individual teeth are of high interest (see also van der Wal, Giesen & Videler, 2000;Ukmar-Godec et al., 2015;Krings et al., 2020b), but in order to link morphology and function it is necessary to understand the radula as a complex functional unit with mechanically interacting, non-independent structures (Morris & Hickman, 1981;Hickman, 1984;Padilla, 2003;Herrera et al., 2015;Krings et al., 2019a). ...
Here, we explore the concept that radular tooth morphology not only reflects the food-gathering function, but might also reflect functional constraints during the folded phase and storage of teeth.
... The hardness and elastic modulus (Young's modulus) relates to the ingesta as well e.g. [33,34] . Radular teeth of some molluscan taxa, Polyplacophora and Patellogastropoda, are very hard and stiff, caused by high proportions of incorporated iron, reducing tooth wear when interacting with algae attached to solid sub-strates [ 3 , 34-47 ]. ...
... As teeth are in direct contact with the ingesta, their morphology can often be directly linked with the animal's ecology and can reflect various transitions from zoovorous to herbivorous traits [101][102][103][104][105][106]. Form together with the tooth's position and chemical composition are widely considered adaptive to food and are hence closely associated with feeding strategies, competitor avoidance and thus trophic specialization [107][108][109][110][111][112][113][114][115][116][117][118]. ...
Background: Lake Tanganyika belongs to the East African Great Lakes and is well known for harbouring a high proportion of endemic and morphologically distinct genera, in cichlids but also in paludomid gastropods. With about 50 species these snails form a flock of high interest because of its diversity, the question of its origin and the evolutionary processes that might have resulted in this elevated amount of taxa. While earlier debates centred on these paludomids to be a result of an intralacustrine adaptive radiation, there are strong indications for the existence of several lineages before the lake formation. To evaluate hy-potheses on the evolution and radiation the detection of actual adaptations is crucial. Since the Tanganyikan gastropods show distinct radular tooth morphologies hypotheses about potential trophic specializations are at hand.
Results: Here, based on a phylogenetic tree of the paludomid species from Lake Tanganyika and adjacent river systems, the mechanical properties of their teeth were evaluated by nanoindentation, a method measuring the hardness and elasticity of a structure, and relat-ed with the gastropods’ specific feeding substrate (soft, solid, mixed). Results identify me-chanical adaptations in the tooth cusps to the substrate and, with reference to the tooth morphology, assign distinct functions (scratching or gathering) to tooth types. Analysing pure tooth morphology does not consistently reflect ecological specializations, but the me-chanical properties allow the determination of eco-morphotypes.
Conclusion: In almost every lineage we discovered adaptations to different substrates, lead-ing to the hypothesis that one main engine of the flock’s evolution is trophic specialization, establishing distinct ecological niches and allowing the coexistence of taxa.
Keywords: Functional morphology, nanoindentation, mechanical properties, Gastropoda, trophic specialisation, adaptive radiation
... Persistent polyamorphism in the chiton tooth: From a new biomineral to inks for additive manufacturing tooth head during the feeding stroke ( Fig. 1D and SI Appendix, Fig. S10 A and B) (19). The stylus connects the tooth head to the radula and orients the tooth with respect to the substratum (20). The radula membrane ( Fig. 1D and SI Appendix, Fig. S10C) has lower stiffness to accommodate complex shape changes but at the same time must be strong, tough, and resistant to fatigue to survive the cycling bending and unbending during feeding. ...
Multimodal Investigation of Chiton Stylus Reveals New Biomineral - Linus Stegbauer, Paul Smeets, Esen Ercan Alp, Derk Joester
... Within the last two decades, material properties of rhipidoglossan and docoglossan radular teeth had been studied extensively in Patellogastropoda and Polyplacophora; it has been shown that different elements, sometimes a substantial amount of iron, is incorporated in the chitinous teeth material making the teeth more wear resistant (e.g. Runham, 1961;Towe et al., 1963;Runham et al., 1969;van der Wal, 1989;Evans et al., 1991Evans et al., , 1992van der Wal et al., 2000;Lee et al., 2003;Brooker et al., 2003;Shaw et al., 2010;Weaver et al., 2010;Brooker and Shaw, 2012;Lu and Barber, 2012;Ukmar-Godec et al., 2015). Since the amount and the composition of embedded elements differ between the previously studied mollusc species, the teeth have different mechanical properties (e.g. ...
One important autapomorphy of molluscs is the radula, which is the anatomical structure used for feeding in most species of Mollusca. As this phylum represents the second species-richest animal group inhabiting very diverse environments, it is not surprising that the morphology of the radula and its teeth is also very diverse between taxa. However, the taenioglossan radulae are remarkable because its tooth types (central, lateral, and marginal teeth) are highly distinct in their morphology within the same radula. There are several hypotheses attempting to explain this tooth diversity by their functional specialisations. Here, for the first time, the functional morphology of taenioglossan radular teeth from one single species was analysed and their material properties (hardness and elasticity modulus) were characterised by nanoindentation. Spekia zonata Bourguignat, 1879 belongs to the Paludomidae inhabiting and feeding on solid substrates in Lake Tanganyika. All tooth types show gradual and significant differences in their stiffness and hardness: from the basis, as the softest and most flexible area, to the stylus and the cusps as the stiffest and hardest areas. The flexibility of the stylus allows the teeth to act as one single feeding organ: the central and lateral teeth can stabilize each other during feeding by the rear teeth providing support to the next row. Tooth types also differ significantly in their stiffness and hardness: the central teeth consist of the hardest and stiffest material, followed by the lateral teeth and finally marginal teeth. This can be explained by different functional loads of teeth: central and lateral ones are used for scratching over the substrate while the marginals serve mainly as brooms collecting food particles.
... Nevertheless, special features of the radula are thought to be linked to particular feeding strategies. The most prominent tooth, the mineralised second lateral, shows not only a varying denticulation among taxa, but also a variable mixture of hardening elements (van der Wal et al., 2000). The different forms of the central tooth also indicate that their different morphology is linked to feeding processes. ...
Seven different ecological feeding strategies have previously been identified among chitons, despite their apparent morphological homogeneity. These include: detrivores, herbivores, omnivorous grazers, carnivorous grazers, specialist spongivores, epizoophagous feeders, xylophagous wood-dwelling species and true predators. The majority of species among common intertidal chitons appear to be omnivorous grazers. Here, we examined the gut morphology, and radula morphology, in species from various feeding types. The proportionate length and mineralization of the radula are not strongly correlated with feeding type, but these characteristics could be refined and later used to exclude particular habits where no other ecological data are available. Gut length in chitons follows classical gut foreshortening, with ambush predators having a short intestinal tract forming a single major loop, whereas obligate herbivores having dramatically long intestinal lengths with multiple coilings. Multiple feeding strategies, and concomitant adaptation of the digestive system, can be observed among phylogenetically closely-related taxa. Niche partitioning through dietary specialization, even among co-occurring omnivorous grazers, may speculatively underpin the success of chitons in the Northeast Pacific and other regions.
Leafcutter ants show a high degree of task division among the workers of different castes. For example, the smallest workers, the minims, care for the brood and the symbiotic fungus, whereas the larger mediae cut and transport plant material. This is reflected in the size and morphology of the mandibles, but also in their mechanical properties as mediae possess the hardest and stiffest cuticle and the minims—the softest and most flexible one. This is directly related to the content of the cross‐linking transition metal zinc (Zn). The cuticle microstructure, which can be more or less anisotropic depending on the orientation of cuticle layers, is known to determine the resistance to loads and stresses and thus contributes to the biomechanical behaviour of the structure. To study how the mandible tasks are related to the cuticular organisation, we here documented the microstructure of the mandibles from the mediae and the minims by scanning electron microscopy. Afterwards, the mechanical properties (Youngs' modulus, E , and hardness, H ) of the exo‐, meso‐ and endocuticle were identified by nanoindentation. Tests were performed along the longitudinal and the circumferential axes of the mandibles. We found, that the minims possess mandibles, which are more isotropic, whereas the mandibles of the mediae are rather anisotropic. This difference was never determined within one species before and is probably linked to the task of the individual ant. To gain insight into the origins of these properties, we characterized the elemental composition of the different cuticle layers along the circumferential axis, revealing that only the exocuticle of the mandible cutting edge contains Zn. All other mechanical property gradients thus must be the result of the chitin fibre bundle architecture or the properties of the protein matrix, which awaits further investigation.
The radula, composed on a chitinous membrane with longitudinal and transversal rows of embedded teeth, is the molluscan autapomorphy for food gathering and processing. Within the Mollusca, this organ is highly diverse in morphology, material composition, and its mechanical properties. We here provide a summary of the known material composition and properties of radular teeth and their relationship with the preferred ingesta, the tooth function and the resistance of structures to failure and wear. In general, multiple mechanisms, e.g. the chemical composition, the micro- and nanostructure of teeth, the underlying supporting structures, or the interplay between structures, contribute to the radular performance. In different molluscan taxa, these mechanisms contribute to different extents to both wear- and failure-reduction (i.e., some teeth possess high contents of metals and minerals whereas, in other taxa, teeth are stiffened and hardened by the degree of cross-linking). This highlights the potential of evolving convergent solutions to common biomechanical constrains at the ingesta processing apparatus.
Chiton articulatus is a species of mollusk living in the tropical Pacific intertidal rocky shores of Mexico. This species feeds on solid waste organic sources, including hard crustose algae that grow on rocky substrates, by grazing on them with its radula, a flexible chitinous membrane lined with mineralized major lateral teeth. In this study, the composition, morphology, and resulting mechanics of the mature teeth of this species, which have yet to be examined, are revealed. The results show the presence of multiphasic mature teeth, each consisting of aligned hard magnetite nanoparticles on the leading edge of the tooth underneath which are magnetite lamellae, followed by goethite, lepidocrocite, and eventually hydroxyapatite near the trailing edge. This multiregional structure demonstrates a gradation in hardness as well as different microstructural features integrated with tough interfaces. The combination of these microstructural and phase arrangements results in an abrasion‐resistant tough structure with a self‐sharpening ability. The results of this work will help contribute to developing new bioinspired designs while also helping to understand the evolution and feeding habits of these intriguing invertebrates.
Insect feeding structures, such as mandibles, interact with the ingesta (food or/and substrate) and can be adapted in morphology, composition of material and mechanical properties. The foraging on abrasive ingesta, as on algae covering rocks, is particularly challenging because the mandibles will be prone to wear and structural failure, thus suggesting the presence of mandibular adaptations to accompany this feeding behavior. Adaptations to this are well studied in the mouthparts of molluscs and sea urchins, but for insects there are large gaps in our knowledge. In this study, we investigated the mandibles of a grazing insect, the larvae of the trichopteran Glossosoma boltoni. Using scanning electron microscopy, wear was documented on the mandibles. The highest degree was identified on the medial surface of the sharp mandible tip. Using nanoindentation, the mechanical properties, such as hardness and Young's modulus, of the medial and lateral mandible cuticles were tested. We found, that the medial cuticle of the tip was significantly softer and more flexible than the lateral one. These findings indicate that a self-sharpening mechanism is present in the mandibles of this species, since the softer medial cuticle is probably abraded faster than the harder lateral one, leading to sharp mandible tips. To investigate the origins of these properties, we visualized the degree of tanning by confocal laser scanning microscopy. The autofluorescence signal related to the mechanical property gradients. The presence of transition and alkaline earth metals by energy dispersive X-ray spectroscopy was also tested. We found Ca, Cl, Cu, Fe, K, Mg, Mn, P, S, Si, and Zn in the cuticle, but the content was very low and did not correlate with the mechanical property values.
Several families of neogastropod mollusks independently evolved the ability to drill through mineralized prey skeletons using their own mineralized feeding teeth, sometimes with shell‐softening chemical agents produced by an organ in the foot. Teeth with more durable tooth shapes should extend their use and improve predator performance, but past studies have described only the cusped‐side of teeth, mostly overlooking morphologies related to functional interactions between teeth. Here, we describe the three‐dimensional morphology of the central drilling tooth (rachidian) from four species of the neogastropod family Muricidae using synchrotron tomographic microscopy and assemble a three‐dimensional model of a multitooth series in drilling position for two of them to investigate their dynamic form. We find two new types of articulating surfaces, including a saddle joint at either end of the rachidian and a large tongue‐and‐groove joint in the center. The latter has a shape that maximizes contact surface area between teeth as they rotate away from each other during drilling. Articulating joints have not been described in Neogastropod radula previously, but they are consistent with an earlier hypothesis that impact forces on individual teeth during predatory drilling are dispersed by tooth–tooth interactions.
The radula, a chitinous membrane with teeth, is the molluscan autapomorphy for food gathering and processing. Even though this structure is studied for decades, the interplay between the structure and the particular food or/and the substrate remains mostly enigmatic. Here, we provide a numerical model approach to understand the relationship between structure, feeding efficiency, and partial work performed by the system. This first simple dynamic numerical radular model interacts with the food particles and the uneven substrate. This protocol can be applied to any system in the future, as the parameters (interaction between structures, adhesion, size of food particles, attachment angle of teeth to membrane, etc.) can be easily altered. This will shed light on the biomechanical adaptations of this feeding structure (e.g., wear and failure prevention) to the specific environment.
Materials displaying negative Poisson’s ratio, referred to as auxeticity, have been found in nature and created in engineering through various structural mechanisms. However, uniting auxeticity with high strength and high stiffness has been challenging. Here, combining in situ nanomechanical testing with microstructure-based modeling, we show that the leading part of limpet teeth successfully achieves this combination of properties through a unique microstructure consisting of an amorphous hydrated silica matrix embedded with bundles of single-crystal iron oxide hydroxide nanorods arranged in a pseudo-cholesteric pattern. During deformation, this microstructure allows local coordinated displacement and rotation of the nanorods, enabling auxetic behavior while maintaining one of the highest strengths among natural materials. These findings lay a foundation for designing biomimetic auxetic materials with extreme strength and high stiffness.
Background: Most molluscs forage with their radula, a chitinous membrane with embedded teeth. As teeth are interfaces between the individual and its ingesta, trophic specialisations can be reflected by morphology, composition, and mechanical properties of the radula. Adaptations to the ingesta – especially with regard to mechanisms contributing to the reduction of structural failure and wear – are well studied in the heavily mineralized teeth of Polyplacophora and Patellogastropoda. For the rather chitinous teeth of non-limpet snails, we are however confronted with a large gap of knowledge.
Results: For this study, we selected nudibranch gastropods, which are of high interest, when studying trophic specialisations, because taxa are strongly adapted to forage on certain prey types. To shed some light on this type of radula, we here investigated two species – Felimare picta and Doris pseudoargus, which are similar with regard to their food preference (Porifera-consuming). Tooth morphologies were documented using scanning-electron-microscopy and mechanical properties were tested by nanoindentation, to develop hypotheses on functional adaptations of the radula to the ingesta. We found
that tooth morphologies and mechanical properties are rather similar in both species, indicating that teeth are similar in their function. In the search for the reasons of the specific mechanical properties, we studied the material composition. Teeth were visualized using confocal laser scanning microscopy (CLSM), to determine the degree of tanning, and analysed with energy-dispersive X-ray spectroscopy (EDX), to determine the elemental composition. Our results show, that the inorganic content and the
emitted autofluorescence signal differ between the species. This was especially prominent, when studying the inner and outer sides (leading and trailing edges) of teeth. In F. picta, we detected high proportions of Si, whereas teeth of D. pseudoargus contained high amounts of Ca, which influenced the autofluorescence signal in CLSM. Using nanoindentation we determined high Young’s modulus and hardness values for the leading edges of teeth, which seem to correlate with the Si- and Ca-content.
Conclusions: This is a new set of data for non-limpet gastropods, rendering that their teeth can be mechanically enhanced via different chemical pathways to reach similar properties in reducing structural failure and abrasion.
Background
The radula, a chitinous membrane with embedded teeth, is one important molluscan autapomorphy. In some taxa (Polyplacophora and Patellogastropoda) one tooth type (the dominant lateral tooth) was studied intensively in the last decades with regard to its mechanical properties, chemical, and structural composition, and the relationship between these parameters. As the dominant lateral tooth is probably one of the best studied biological materials, it is surprising, that data on chemistry and mechanical properties of the other tooth types, present on a chiton radula, is lacking.
Results
We provide data on the elemental distribution and mechanical properties (hardness and elasticity, i.e. Young’s modulus) of all teeth from the Polyplacophora Lepidochitona cinerea (Linnaeus, 1767) [Chitonidae: Ischnochitonidae]. The ontogeny of elements, determined by energy-dispersive X-ray spectroscopy, and of the mechanical properties, detected by nanoindentation, was studied for every single tooth type. Additionally, we performed breaking stress experiments with teeth under dry and wet condition, highlighting the high influence of the water content on the mechanical behaviour of the radula. We thereby could determine the forces and stresses, teeth can resist, which was previously not studied in representatives of Polyplacophora. Overall, we were able to relate the mineral (iron, calcium) content, the mechanical parameters, breaking force, and stress for each tooth type. This led to a better understanding of the relationship between structure, material, and function in radular teeth. Further, we aimed at determining the role of calcium for the mechanical behaviour of the teeth: we decalcified radulae by ethylenediaminetetraacetic acid and afterwards performed elemental analyses, breaking stress experiments and determined the mechanical properties. Among other things, we detected that wet and decalcified radular teeth could resist highest forces, since teeth have a higher range of bending motion leading to a higher capability of teeth to gain mechanical support from the adjacent tooth row.
Conclusion
We present novel data on the chemistry, mechanical properties, and the mechanical behaviour of chiton teeth, which allows conclusions about tooth function. We could also relate the parameters mentioned, which contributes to our understanding on the origins of mechanical property gradients and the processes reducing structural failure in radular teeth.
The radula is the structure used for food processing in Mollusca. It can consist of a membrane with stiffer teeth, which is, together with alary processus, muscles and odontophoral cartilages, part of the buccal mass. In malacology, it is common practice to infer potential tooth functions from morphology. Thus, past approaches to explain functional principles are mainly hypothesis driven. Therefore, there is an urgent need for a workflow testing hypotheses on the function of teeth and buccal mass components and interaction of structures, which can contribute to understanding the structure as a whole. Here, in a non-conventional approach, we introduce a physical and dynamic radular model, based on morphological data of Spekia zonata (Gastropoda, Paludomidae). Structures were documented, computer-modelled, three-dimensional-printed and assembled to gather a simplistic but realistic physical and dynamic radular model. Such a bioinspired design enabled studying of radular kinematics and interaction of parts when underlain supporting structures were manipulated in a similar manner as could result from muscle contractions. The presented work is a first step to provide a constructional manual, paving the way for even more realistic physical radular models, which could be used for understanding radular functional morphology and for the development of novel gripping devices.
The radula, a chitinous membrane with embedded tooth rows, is the molluscan autapomorphy for feeding. The morphologies, arrangements and mechanical properties of teeth can vary between taxa, which is usually interpreted as adaptation to food. In previous studies, we proposed about trophic and other functional specialisations in taenioglossan radulae from species of African paludomid gastropods. These were based on the analysis of shape, material properties, force-resistance, and the mechanical behaviour of teeth, when interacting with an obstacle, which was previously simulated for one species ( Spekia ) by the finite-element-analysis (FEA) and, for more species, observed in experiments. In the here presented work, we test the previous hypotheses by applying the FEA on 3D modelled radulae, with incorporated material properties, from three additional paludomid species. These species forage either on algae attached to rocks ( Lavigeria ), covering sand ( Cleopatra ), or attached to plant surface and covering sand ( Bridouxia ). Since the analysed radulae vary greatly in their size between species, we additionally aimed at relating the simulated stress and strain distributions with the tooth sizes by altering the force/volume. For this purpose, we also included Spekia again in the present study. Our FEA results show that smaller radulae are more affected by stress and strain than larger ones, when each tooth is loaded with the same force. However, the results are not fully in congruence with results from the previous breaking stress experiments, indicating that besides the parameter size, more mechanisms leading to reduced stress/strain must be present in radulae.
The molluscan radula, a thin membrane with embedded rows of teeth, is the structure for mechanical food processing and gathering. For proper functioning, radular failures must be either avoided or reduced, as this might be of high significance for the individual fitness. The factors, leading to the structural failure of teeth, are related to trophic specializations of species. Here, the failure of non-mineralized, chitinous radular teeth from an African paludomid species flock, inhabiting Lake Tanganyika and surrounding river systems, were tested in a biomechanical experiment. These species are of high interest for evolutionary biologists, since they represent a potential result of an adaptive radiation. With a force transducer attached to a motorized stage, a shear load was applied to tooth cusps until structural failure occurred. Subsequently broken areas were measured, and breaking stress was calculated. As the experiments were carried out under dry and wet conditions, the high influence of the water content on the forces, teeth were capable to resist to, could be documented. Wet teeth were able to resist to higher forces, because their flexibility was higher, which enabled them either to slip away or to gain support from adjacent teeth. This mechanism can be understood as collective effect reducing structural failure, without the mineralisation by wear-minimizing elements, as described for Polyplacophora and Patellogastropoda. As the documented mechanical behaviour of radular teeth is related to the gastropod ecological niche, it can thus be identified as an adaptation to preferred feeding substrates.
It is available here:
https://papers.ssrn.com/sol3/papers.cfm?abstract_id=3828270
We report the electron microscopy-based analysis of the major lateral tooth of the limpet Colisella subrugosa during early and intermediate stages of development. We aimed to analyze the structural relationship among the needle-like crystals of the iron oxide goethite, the amorphous silica phase that forms the tooth base and occupy inter-crystalline spaces in the cusp, and the chitin fibers of the matrix. Goethite crystals followed the three dimensional organization pattern of the chitin fibers in the cusp. In the tooth base, spherical individual silica granules were found in regions where the chitin fibers cross. The spherical granules near the interface between the tooth base and the cusp (junction zone) formed an almost continuous medium that could easily be ultrathin-sectioned for further analysis. By contrast, the nearby silica-rich region localized on the other side of the junction zone contained needle-like goethite crystals immersed in the matrix and presented a conchoidal fracture. The chitin fibers from the silica granules of the tooth base were dotted or undulating in projection with a periodicity of about 6 nm when observed by high magnification transmission electron microscopy. Very thin goethite crystals were present in the base of the cusp near the junction zone surrounded by silica. On several occasions, crystals presented internal thin straight white lines parallel to the major axis, indicating a possible growth around fibers. We propose that silica and iron oxide phases mineralization may occur simultaneously at least for some period and that silica moderates the dimensions of the iron oxide crystals.
https://ediss.sub.uni-hamburg.de/handle/ediss/8654
The radula is the anatomical structure used for feeding in most Mollusca species and is
one important autapomorphy. Previous studies were focused on the radular teeth and their functional morphology, but their anchorage in the radular membrane and its function have never been examined. Here, we analyse the micro-structure of connecting chitinous fibres and its implication on the radular function in 13 closely related paludomid gastropod species from the so called “ancient lake” Tanganyika. This species flock shows a stunning interspecific diversity in their radular tooth morphology and tooth embedding in the membrane as well. The species studied here feed on organics from different substrates, both soft and solid, and are substrate-specific. Here, the morphological composition of the membrane is described in detail for the first time, it consists of parallel fibres that extend also within the teeth. We also show that morphologies of the anchorage correlated with the specific preferred feeding substrate can hence be identified as functional adaptation.
Chitons are herbivorous invertebrates that use rows of ultrahard magnetite-based teeth connected to a flexible belt (radula) to rasp away algal deposits growing on and within rocky outcrops along coastlines around the world. Each tooth is attached to the radula by an organic structure (stylus) that provides mechanical support during feeding. However, the underlying structures within the stylus, and their subsequent function within the chiton have yet to be investigated. Here, we investigate the macrostructural architecture, the regional material and elemental distribution and subsequent nano-mechanical properties of the stylus from the Northern Pacific dwelling Cryptochiton stelleri. Using a combination of μ-CT imaging, optical and electron microscopy, as well as elemental analysis, we reveal that the stylus is a highly contoured tube, mainly composed of alpha-chitin fibers, with a complex density distribution. Nanoindentation reveals regiospecific and graded mechanical properties that can be correlated with both the elemental composition and material distribution. Finite element modeling shows that the unique macroscale architecture, material distribution and elemental gradients have been optimized to preserve the structural stability of this flexible, yet robust functionally-graded fiber-reinforced composite tube, providing effective function during rasping. Understanding these complex fiber-based structures offers promising blueprints for lightweight, multifunctional and integrated materials.
The radula is the anatomical structure used for feeding in most species of Mollusca. Previous studies have revealed that radulae can be adapted to the food or the substrate the food lies on, but the real, in vivo forces exerted by this organ on substrates and the stresses that are transmitted by the teeth are unknown. Here, we relate physical properties of the radular teeth of Cornu aspersum (Müller. 1774 Vermium terrestrium et fluviatilium, seu animalium infusoriorum, helminthicorum, et testaceorum, non marinorum, succincta historia. Volumen alterum. Heineck & Faber, Havniæ & Lipsiæ.), a large land snail, with experiments revealing their radula scratching force. The radula motion was recorded with high-speed video, and the contact area between tooth cusps and the substrate was calculated. Forces were measured in all directions; highest forces (106.91 mN) were exerted while scratching, second highest forces while pulling the radula upwards and pressing the food against its counter bearing, the jaw, because the main ingesta disaggregation takes place during those two processes. Nanoindentation revealed that the tooth hardness and elasticity in this species are comparable to wood. The teeth are softer than some of their ingesta, but since the small contact area of the tooth cusps (227 µm2) transmits high local pressure (4698.7 bar) on the ingesta surface, harder material can still be cut or pierced with abrasion. This method measuring the forces produced by the radula during feeding could be used in further experiments on gastropods for better understanding functions and adaptations of radulae to ingesta or substrate, and hence, gastropods speciation and evolution.
Limpets are marine mollusks using mineralized teeth, one of the hardest and strongest biomaterials, to feed on algae on intertidal rocks. However, most of studies only focuses on the ultrastructure and chemical composition of the teeth while the molecular information is largely unknown, limiting our understanding of this unique and fundamental biomineralization process. In this study, we investigated the microstructure, proteomics and crystallization in the teeth of limpet Cellana toreuma. It is found that the limpets formed alternatively tricuspid teeth and unicuspid teeth. Small nanoneedles were densely packed at the tips or leading regions of the cusps. In contrast, big nanoneedles resembling chemical synthesized goethite were loosely packed in the trailing regions of the cusps. Proteins extracted from the whole radula such as ferritin, peroxiredoxin, arginine kinase, GTPase‐Rabs and clathrin were identified by proteomics. Goethite‐binding experiment coupled with proteomics and RNA‐seq highlighted six chitin‐binding proteins (CtCBPs). Furthermore, the extracted proteins from the cusps of radula or the framework chitin induced packing of crystals and possibly affected crystal polymorphs in vitro. This study provides insight into the unique biomineralization process in the limpet teeth at the molecular levels, which may guide biomimetic strategies aimed at designing hard materials at room temperature.
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Biological material systems have evolved unique combinations of mechanical properties to fulfill their specific function through a series of ingenious designs. Seeking lessons from Nature by replicating the underlying principles of such biological materials offers new promise for creating unique combinations of properties in man‐made systems. One case in point is Nature's means of attack and defense. During the long‐term evolutionary “arms race,” naturally evolved weapons have achieved exceptional mechanical efficiency with a synergy of effective offense and persistence—two characteristics that often tend to be mutually exclusive in many synthetic systems—which may present a notable source of new materials science knowledge and inspiration. This review categorizes Nature's weapons into ten distinct groups, and discusses the unique structural and mechanical designs of each group by taking representative systems as examples. The approach described is to extract the common principles underlying such designs that could be translated into man‐made materials. Further, recent advances in replicating the design principles of natural weapons at differing lengthscales in artificial materials, devices and tools to tackle practical problems are revisited, and the challenges associated with biological and bioinspired materials research in terms of both processing and properties are discussed. The critical structural and mechanical designs employed by naturally evolved weapons in pursuing their high mechanical efficiency in Nature's evolutionary arms race are reviewed. The materials‐design strategies towards an outstanding synergy of offence and persistence are extracted from such weapons. The challenges and opportunities associated with natural weapons in biological and bioinspired materials research are discussed.
Teeth are designed to deliver high forces while withstanding the generated stresses. Aside from isolated mineral-free exception (e.g., marine polychaetes and squids), minerals are thought to be indispensable for tooth-hardening and durability. Here, the unmineralized teeth of the giant keyhole limpet (Megathura crenulata) are shown to attain a stiffness, which is twofold higher than any known organic biogenic structures. In these teeth, protein and chitin fibers establish a stiff compact outer shell enclosing a less compact core. The stiffness and its gradients emerge from a concerted interaction across multiple length-scales: packing of hydrophobic proteins and folding into secondary structures mediated by Ca(2+) and Mg(2+) together with a strong spatial control in the local fiber orientation. These results integrating nanoindentation, acoustic microscopy, and finite-element modeling for probing the tooth's mechanical properties, spatially resolved small- and wide-angle X-ray scattering for probing the material ordering on the micrometer scale, and energy-dispersive X-ray scattering combined with confocal Raman microscopy to study structural features on the molecular scale, reveal a nanocomposite structure hierarchically assembled to form a versatile damage-tolerant protein-based tooth, with a stiffness similar to mineralized mammalian bone, but without any mineral.
The materials mechanics of the controlled separation of a body into two or more parts - cutting - using a blade or tool or other mechanical implement is a ubiquitous process in most engineering disciplines. This is the only book available devoted to the cutting of materials generally, the mechanics of which (toughness, fracture, deformation, plasticity, tearing, grating, chewing, etc.) have wide ranging implications for engineers, medics, manufacturers, and process engineers, making this text of particular interest to a wide range of engineers and specialists. * The only book to explain and unify the process and techniques of cutting in metals AND non-metals. The emphasis on biomaterials, plastics and non-metals will be of considerable interest to many, while the transfer of knowledge from non-metals fields offers important benefits to metal cutters * Comprehensive, written with this well-known author's lightness of touch, the book will attract the attention of many readers in this underserved subject * The clarity of the text is further enhanced by detailed examples and case studies, from the grating of cheese on an industrial scale to the design of scalpels.
SUMMARY The indentation hardness of locust cuticle was measured using a Vickers diamond applied to the surface of the cuticle. A number of areas of cuticle showed similar hardness values, approximately 24 kg mm~!, for the de- hydrated cuticle but the mandibles (298 kg mm 4) and the dorsal meso- thorax (33-3 kg mm 4) were harder. The mandibles have localized areas of hardness which are related to their function. It is suggested that the hardness of the dorsal thorax may be related to its function as an energy storing structure in flight. The measured hardness of cuticle depends on the hydration of the material but relative differences between cuticles from different parts of the locust persist whether tested fresh or after dehydration. Hardness is correlated with the dihydroxyphenol content of cuticle (unlike stiffness), conversely it is not correlated with the hydrophobicity of the matrix proteins (unlike stiffness). It is emphasized that hardness and stiffness are very different mechanical properties.
Acoustic microscopy enables one to image the interaction of acoustic waves with the elastic properties of a specimen with microscopic resolution. A lens with good focusing properties on the axis can be used for both transmitting and receiving the signal, and an image is formed by scanning the lens mechanically over the specimen. In pressurised superfluid helium with nonlinear coupling to harmonics a resolution of 15 nm has been achieved, but for routine use 2 GHz is the highest practical frequency, which offers a resolution of about 0.7 mu m. The information is contained in the way that the acoustic wave is reflected from the specimen. For subsurface imaging, especially in polymer based materials such as composites and electronic packaging, the enhanced depth resolution of a confocal imaging system can be exploited to give good contrast from the plane of interest even when the specimen contains many scatters. In higher stiffness specimens, including most metals, semiconductors and ceramics, a dominant role in the contrast can be played by Rayleigh waves in the surface. If the specimen has a surface layer, then the propagation of the Rayleigh waves is sensitive to the perturbing action of the layer. If the specimen is anisotropic, then there will be a dependence on the orientation of the surface and the direction of propagation in it. If there are surface cracks or boundaries, then there will be strong contrast when they scatter the Rayleigh waves. Detailed theory is available to relate the elastic properties of the surface to the contrast, and these enable informed interpretation of the acoustic images to be made, and also provide a foundation for more quantitative acoustic microscopy.
Iron oxide biomineralization in the radula teeth of the common limpet
(Patella vulgata) has been studied by Mossbauer spectroscopy and high
resolution transmission electron microscopy. The results indicate that
the teeth comprise two iron-containing phases: (i) a superparamagnetic,
microcrystalline and poorly ordered goethite-like component located
essentially within the tooth bases; and (ii) stoichiometric well-ordered
goethite crystals of acicular morphology sited within the tooth cusps.
The goethite crystals are initially deposited in the form of long thin
fibrous single crystals elongated along the [001] direction and with
extensive irregularities in crystal thickness. Mature crystals often
show morphological distortions that are not associated with localized
structural imperfections or domain boundaries. The implications of these
results in terms of tooth development are discussed.
The purpose of this Handbook is to provide, in highly accessible form, selected critical data for professional and student solid Earth and planetary geophysicists. Coverage of topics and authors were carefully chosen to fulfill these objectives. These volumes represent the third version of the "Handbook of Physical Constants." Several generations of solid Earth scientists have found these handbooks' to be the most frequently used item in their personal library. The first version of this Handbook was edited by F. Birch, J. F. Schairer, and H. Cecil Spicer and published in 1942 by the Geological Society of America (GSA) as Special Paper 36. The second edition, edited by Sydney P. Clark. Jr., was also published by GSA as Memoir 92 in 1966. Since 1966, our scientific knowledge of the Earth and planets has grown enormously, spurred by the discovery and verification of plate tectonics and the systematic exploration of the solar system.
Scanning electron microscopy was employed to study the ultrastructure of the magnetite-bearing cap in mature tricuspid teeth of four chiton species: Lepidochitona cinerea, Mopalia muscosa, Katharina tunicata, and Cryptochiton stelleri. The cap is composed of parallel rod-shaped units. In the part that leads in the cutting direction there are two sets of intersecting structural units. In the trailing part a single set of units occurs. The construction of the cap in relation to its function is discussed.
The geometry and character of minerals in young mineralizing teeth of Cryptochiton stelleri were studied by transmission and high resolution transmission electron microscopy. Ferrihydrite is the first mineral species formed during the mineralization process. It is precipitated in clusters of elongate, parallel crystals. Next, magnetite crystals appear along the edges of the ferrihydrite clusters. During further growth the magnetite crystals enlarge, whereas simultaneously the ferrihydrite crystals gradually disappear. It is discussed that the mineralization process proceeds in tubular compartments with walls composed of organic materials, which develop into the rod-shaped units constituting the magnetite-bearing cap in mature teeth.
Scanning acoustic microscopy is a form of microscopy based on the generation and detection of elastic waves in solids. The basic mechanism is the interaction of an acoustic wave with a specimen and the consequent generation of acoustic waves inside the material. Such interaction is characteristically different from optical or electronic interactions, and is mainly dependent on the mechanical properties of the specimen. As a consequence, acoustic microscopy provides an important and complementary source of information for the examination of materials. Two major advantages are obtained using an acoustic microscope. First, acoustic waves are capable of penetrating materials that are opaque to other kinds of radiation. As a result, the acoustic microscope can image subsurface characteristics of materials without the necessity of etching or coating the surface of the sample. The second advantage relies on the origin of contrast in acoustic microscopy lying in the interaction of elastic waves with local variations in mechanical properties. Using an acoustic microscope it is therefore possible to study, with high resolution and sensitivity, mechanical properties of the specimen such as density, elasticity, and viscosity. In the field of material science, applications of acoustic microscopy are quite wide and range from the analysis of cracks and other defects in engineering materials to the study of integrated circuits and electronic components. Moreover, recent advances in quantitative acoustic microscopy enable the determination of mechanical material parameters on a microscopic scale.
Magnetite was first identified as a biogenic mineral in the radula teeth of chitons (Mollusca, Polyplacophora) (Lowenstam, 1962). The caps of mature major lateral teeth are composed in part of crystalline magnetite in an ordered matrix of organic fibrils (Towe and Lowenstam, 1967; Kirschvink and Lowenstam, 1979). The biomineralization proceeds in two steps: (1) an initial deposition of ferrihydrite (5Fe2O3•9H2O) (Towe and Bradley, 1967) within the organic matrix of the tooth cap (Towe and Lowenstam, 1967), and (2) the transformation of the ferrihydrite into magnetite (FeO•Fe2O3) (Towe and Lowenstam, 1967).
H F Pollard London: Pion 1977 (distrib. by Academic) pp xiii + 366 price ?10.50
Acoustical techniques are employed increasingly in investigations of the solid state, with their wide industrial applications to nondestructive testing. The gathering together of this information with the necessary basic theoretical background in a book of 366 pages demands careful selection and presentation.
The article describes the evolution of a simple model assuming a pyramidal point for determining the efficiency with which an abrasive removes material from a workpiece.
Preliminary data are presented on the physical properties and the mineralogy of the material in denticle caps of chitons. The X-ray diffraction patterns of the denticle material indicate the presence of magnetite, or possibly maghemite. This is the first indication that magnetite or possibly maghemite is precipitated by a biologic agent in sea water. Hence, the origin of magnetite reported in recent and fossil marine deposits will have to be re-examined. The hardness of the denticle material (Ca. 6 on the Mohs scale) explains why chitons are effective erosional agents of rock surfaces, particularly of limestone. From the biologic point of view the possibility is considered that the magnetic properties of the denticle caps may serve as a guidance system for the so-called homing instinct of chitons.
Phosphatic substances are described from hard tissues of species from seven classes of marine invertebrates. Francolite is identified in the species of one class and amorphous calcium- and ferric phosphates, apparently in the form of hydrogels, are recognized as precipitates of species from six other classes. Considering all known phosphatic substances in animal hard parts, it is found that amorphous constituents are far more common in invertebrates than crystalline compounds. The role of amorphous precipitates in providing physical strength to hard parts is examined. Brief comparison is made between phosphate fixation in the phyla spectrum of recent and fossil invertebrates.
The structure, morphology, composition, and organization of inorganic solids in the radula teeth of the limpet Patella vulgata have been studied by electron microscopy, electron diffraction, and e.d.X.a. of fractured, acid-treated, and sectioned tissue. Minerals first appear in the tooth base and comprise: amorphous and poorly crystalline granular, particulate, and sheet-like phases of variable composition (Fe, Si, P, Ca); irregular laths of crystalline goethite; and single crystals of prismatic goethite. The presence of localized Si and P may inhibit goethite crystallization in many regions of the tooth base. Mineralization of the tooth cusp begins with goethite impregnation of the posterior region. Crystals are deposited in the form of thin fibrous strands (15-20 nm width) with the [001] crystallographic axis initially parallel to the posterior tooth wall. Mineralization proceeds by an increase in the number and thickness of the crystals within the posterior region. In contrast, the anterior zone is only partly impregnated with crystals aligned parallel to the long axis of the cusp. The mature crystals are well ordered, acicular in morphology but with extensive growth distortions, and organized along regularly interspaced (30-50 nm) electron-dense filaments within the cusp. Removal of iron reveals the presence of silica-impregnated fibres, folded sheets, and tubular structures (often 30-60 nm in diameter) within essentially intact teeth. We propose that goethite crystallization and organization is regulated, in part, by spatial constraints established by an ordered filamentous organic matrix and that silica impregnates the matrix components at a later stage in mineralization thus maintaining the structural integrity of the organic tissue.
The radula apparatus in chitons (Polyplacophora) is a toothed ribbon used to excavate algae living on and in rocky substrates. Magnetite (Fe3O4) is a component of mineralized radula teeth. It is contained in a layer beneath the surface that leads in the cutting direction. The architecture and composition of this layer in fully mineralized teeth of Chiton olivaceus were studied by scanning electron microscopy. Worn, broken, sectioned, and etched teeth were examined. Etching was done with 4N HCl or by incubating teeth in cultures of bacteria that exclusively used chitin as a source of carbon and energy.
The magnetite-bearing layer is composed of closely packed rod-shaped and elongated concavo-convex (trough-shaped) units oriented at right angles to the cutting edge making an angle with the leading surface of about 60°. Near the leading surface extensions of these units curve baseward over an angle of about 90°. During the excavating action of the radula wear predominantly occurs through fracturing along the boundaries between the elongated units. This implies that the angle between the surface of wear and the leading surface, the wedge angle, is determined by the internal structure of the tooth and is fixed at about 60°. It is discussed that the microanatomical design of the magnetite-bearing layer is such that during wear material losses are minimized.
Magnetite occurs in granular form and approximately comprises 97% by weight of the magnetite-bearing layer. Chitin is a component of the organic matrix surrounding the mineral grains and forming the boundary layer of the elongated units.
The microscopic determination of ore minerals presents many more
problems than are associated with the recognition of transparent species. It is
shown that accurate measurements of reflectivity and indentation hardness are
sufficiently reproducible to form the basis of a systematic scheme of
identification that is easy to apply and is more reliable than any other at
present, The reflectivity and hardness measurements are made on the same mineral
grain and each takes less than one minute. Subsidiary properties used in the
system include color, anisotropism, pleochroism, and dispersion of the
reflectivity. All ore samples examined so far can be identified without use of
chemical methods. (auth)
The molluscan radula is a cutting apparatus employed in feeding. It is a toothed ribbon located in the mouth cavity. This study focuses on the characterization, organization, and hardness of the various components in full grown, mineralized, radula teeth of the common limpet Patella vulgata. Three major components are identified: Fibrous organic material, acicular crystals of goethite (α-FeOOH), and silica (SiO2). Each forms a coherent network intertwined with the other two. The goethite crystals lie parallel to the fibers in the organic framework. The orientations of fibers and crystals are described in detail. The hardness of the leading part, i.e., the part that leads in the cutting direction, is about twice the hardness in the trailing part. It is argued that this difference results from the greater compactness of the mineral matter in the leading part. The function of the tooth as a cutting device is discussed on the basis of the data presented in this study.
The high silicon content of certain radular sites of the Patellacea (Mollusca, Gastropoda) is shown by infrared absorption
spectrums to be fixed in the form of the mineral opal. Opal and goethite mineralize the cusps and bases of the teeth. The
presence of opalized base plates only in the families Acmaeidae and Lepetidae appears to be of taxonomic significance. Minimum
values of the volume of fixation and of the turnover rate of opal by the Patellacea are calculated to assess the role of this
previously neglected taxon in biological fixation of silica in the oceans. The significance of these organisms points to the
much needed study of the silica transport system in tissue-grade Metazoa.
The critical angle reflection technique was used to determine longitudinal and shear sonic velocity components in the exposed surface of bovine incisors along the tooth axis and perpendicular to it. By grinding a flat on the tooth surface successive layers were exposed and the velocity components measured. Plots of the velocity variation with depth were prepared which show some variation in the enamel, much less in the dentine and a sharp drop at the dentino-enamel junction. Strong evidence of anisotropy is demonstrated, especially in enamel.
X-ray diffraction patterns show that the mature denticles of three extant chiton species are composed of the mineral lepidocrocite
and an apatite mineral, probably francolite, in addition to magnetite. Each of the three minerals forms a discrete microarchitectural
unit of the chiton denticles. This is the first indication that lepidocrocite is precipitated by marine organisms and an apatite
mineral by chitons.
A study of the mineralization processes of the radular teeth in Cryptochiton stelleri shows that the iron minerals are precipitated inside an organic matrix which forms an open-mesh framework. In the immature teeth, the earliest detected phase of mineralization consists of a new ferric compound whose structure remains to be determined. In the mature teeth phase, transformation leads to a change from the ferric mineral to magnetite (Fe2O3 · FeO). Crystalline and paracrystalline ferritin granules occur within the epithelial cells associated with the immature teeth.
The x-ray diffraction patterns of the denticle material from several species show that the material consists of the mineral
goethite. This is the first indication that goethite is precipitated by marine invertebrates. The mineralogy of the denticle
caps has biologic and geologic implications.
A comparison of infrared spectra from individual teeth along the radula of a chiton (Polyplacophora, Mollusca) shows that the first-formed calcium phosphate mineral is amorphous. Over a period of weeks the mineral transforms to dahllite. The c axes of the dahllite crystals are aligned approximately perpendicular to the tooth surface.
Three-dimensional object reconstruction by improved stereo-micrometry
- G Boom
Boom, Three-dimensional object reconstruction by improved
stereo-micrometry, Proc. Fifth European Congress on Electron Microscopy, 1972, pp. 364–365.
- P Õan
P. Õan der Wal et al.r Materials Science and Engineering C 7 2000 129–142