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. 2015 Dec;192(3):392-402.
doi: 10.1016/j.jsb.2015.09.021. Epub 2015 Oct 3.

The giant keyhole limpet radular teeth: A naturally-grown harvest machine

Tina Ukmar-Godec  1 , Gregor Kapun  2 , Paul Zaslansky  3 , Damien Faivre  4
Affiliations

The giant keyhole limpet radular teeth: A naturally-grown harvest machine

Tina Ukmar-Godec et al. J Struct Biol. 2015 Dec.

Abstract

The limpet radula is a feeding organ, which contains more than 100 rows of teeth. During their growth the teeth mature and advance in position along the radula. The simpler doccoglossan radulae operate by grinding rocky substrates, extracting the algae by rasping and scraping with the teeth functioning as shovels. Less is known about the rhipidoglossan radulae, used as rakes or brooms that brush and collect loose marine debris. This type of radula is found in the giant keyhole limpet (Megathura crenulata). The large size of this organism suggests that the rhipidoglossan radula entails a technological superiority for M. crenulata in its habitat. The structure and function of the radulae teeth have however not been reported in detail. Using a combination of 2D and 3D microscopy techniques coupled with amino acid analysis and X-ray scattering, we reveal the working components of M. crenulata's radula. It is characterized by numerous marginal teeth surrounding a pair of major hook-like lateral teeth, two pairs of minor lateral teeth and a large central tooth. The mature major lateral teeth show pronounced signs of wear, which gradually increase towards the very front end of the radula and are evidence for scraping. An abrupt change in the amino acid composition in the major lateral teeth and the concurrent formation of a chitinous fiber-network mark the onset of tooth maturation. In comparison to the simpler rock-scraping doccoglossate limpets, the radula of M. crenulata forms an elaborate feeding apparatus, which can be seen as a natural harvest machine.

Keywords: Amino acid analysis; Electron microscopy; Giant keyhole limpet; Megathura crenulata; Micro-CT; Rhipidoglossan radula; X-ray scattering.

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Figures

Fig. 1
Fig. 1
(a) Schematic of the limpet radula in feeding action. The blue arrow denotes the direction of radula movement during the stroke. (b) A photograph of extracted radula of three adult giant keyhole limpets depicting the inter-specimen variability. (c) Optical micrograph of the mature end of the radula.
Fig. 2
Fig. 2
Schematic representations of the two major types of herbivorous limpet radulae: (left) doccoglossane radula and (right) rhipidoglossane radula. The abbreviations denoting various teeth are: MT = marginal teeth, LT = lateral teeth, mLT = minor lateral teeth, MLT = major lateral teeth and R = central or rachidian tooth.
Fig. 3
Fig. 3
(a) SEM micrograph of the mature end of the Mcren rhipidoglossan radula (compare with schematic in Fig. 2). The major lateral teeth in the first few rows are missing. (b) Optical micrograph of the mature region of the radula focusing on the large R tooth and mLT. (c) Optical micrograph of the mature region of the radula focusing on MLT. (a–c) abbreviated same as in Fig. 2. The scale bars correspond to 500 μm.
Fig. 4
Fig. 4
(a) μCT image of the mature end of the radula. (b) Longitudinal section of two consecutive mature major lateral teeth. (c) SEM micrograph of an extracted mature major lateral tooth. (d) Optical micrograph of an extracted row of inter-locked mature major lateral teeth. (e) SEM micrograph of a mature R tooth enclosed by 4 unicuspid mLT. The arrows point at the two external underdeveloped mLT (abbreviated same as in Fig. 2). (f) μCT images of a longitudinal cross-section of the mature end of radula with the central tooth marked in red. (g) SEM micrograph of mature marginal teeth. Inset: a magnification depicting smaller hair-like structures (denoted by the arrow) covering the surface of marginal teeth. The scale bars in (a–g) are all 500 μm. The scale bar in the inset of (g) is 50 μm. The scale bar in the μCT image (a) is used as a guide to the eye.
Fig. 5
Fig. 5
A μCT image of a pair of consecutive major lateral dicuspid teeth from three different perspectives. Red arrows depict the measured distances.
Fig. 6
Fig. 6
SEM images of the (a) immature, (b) maturing and (c) mature part of the radula. (d and e) Optical micrographs of various stages of maturation of the major lateral tooth: (d) immature stage, (e) transition between immature and maturing and (f) mature stage of the teeth. The SEM and optical images correspond to different radulae, respectively. The red full and dashed circles denote the minor and major cusp of the dominant lateral tooth respectively. The scale bars are 500 μm.
Fig. 7
Fig. 7
The relative amino acid composition of proteins in (a) immature, (b) maturing and (c) mature teeth.
Fig. 8
Fig. 8
Scattering intensity from the (0 1 3) reflection of α-chitin in major lateral teeth: (a) transition region between immature and maturing teeth (see Fig. 6e), (b) early mature tooth and (c) extensively worn mature tooth. The intensities in (a–c) are normalized to a common scale in order to allow for a relative comparison of the chitin content. The scale bar corresponds to 200 μm.
Fig. 9
Fig. 9
(a) Optical micrograph of the major lateral tooth in the scraping and worn tooth developmental stage. (b and c) depict optical micrographs of longitudinal sections of an extensively worn versus a less worn tooth in the scraping region. (d and e) depict SEM images of a tip of a worn tooth. (f) SEM image of an intact mature tooth tip. The worn and intact tooth cusps are marked by full and dashed lines, respectively.
Fig. 10
Fig. 10
(a–c) SEM micrographs of the large tooth in the immature, maturing and mature stages, respectively. (d) SEM micrograph of the central tooth in a late mature stage showing prominent signs of wear. Scale bar corresponds to 200 μm.
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