Plicidentine in the oral fangs of parrotfish (Scarinae, Labriformes)

Abstract

Parrotfish play important ecological roles in coral reef and seagrass communities across the globe. Their dentition is a fascinating object of study from an anatomical, functional and evolutionary point of view. Several species maintained non-interlocked dentition and browse on fleshy algae, while others evolved a characteristic beak-like structure made of a mass of coalesced teeth that they use to scrape or excavate food off hard limestone substrates. While parrotfish use their highly specialized marginal teeth to procure their food, they can also develop a series of large fangs that protrude from the upper jaw, and more rarely from the lower jaw. These peculiar fangs do not participate in the marginal dentition and their function remains unclear. Here we describe the morphology of these fangs and their developmental relationship to the rest of the oral dentition in the marbled parrotfish (Leptoscarus vaigiensis), the star-eye parrotfish (Calotomus carolinus), and the palenose parrotfish (Scarus psittacus). Through microtomographic and histological analyses, we show that some of these fangs display loosely folded plicidentine along their bases, a feature that has never been reported in parrotfish. Plicidentine is absent from the marginal teeth and is therefore exclusive to the fangs. Parrotfish fangs develop a particular type of simplexodont plicidentine with a pulpal infilling of alveolar bone at later stages of dental ontogeny. The occurrence of plicidentine and evidence of extensive tooth wear, and even breakage, lead us to conclude that the fangs undergo frequent mechanical stress, despite not being used to acquire food. This strong mechanical stress undergone by fangs could be linked either to forced contact with congeners or with the limestone substrate during feeding. Finally, we hypothesize that the presence of plicidentine in parrotfish is not derived from a labrid ancestor, but is probably a recently evolved trait in some parrotfish taxa, which may even have evolved convergently within this subfamily.

Keywords: Labridae; Scarinae; dentition; ecomorphology; evolution; functional anatomy; parrotfish; plicidentine.

FIGURE 1

Phylogeny of Scarinae and images of the 3 parrotfish species studied in this article. (a) The phylogeny (adapted from Kazancioğlu et al. (2009) and Baliga & Law (2016)) includes the 10 extant genera of parrotfish grouped within the subfamily Scarinae (red bar) as well as their sister group, the subfamily Cheilinae. Scarine fish are subdivided into two groups: the tribe Sparisomatini (green bar) and the tribe Scarini (blue bar). Parrotfish genera that lack supra‐marginal or distal fangs are marked with an asterisk. (b) Leptoscarus vaigiensis TP, specimen MBIO1853, Standard Length (SL): 245 mm. (c) Calotomus carolinus TP, specimen MBIO1452, SL: 273 mm. (d) Scarus psittacus TP, specimen MBIO890, SL: 200 mm. (b, c, d) Fish photographs were taken by Jeffrey T. Williams, National Museum of Natural History, Smithsonian Institution, and come from the French Polynesia Fish Barcoding Database (http://fishbardb.criobe.pf).

FIGURE 2

Organization of the premaxillary dentition in an adult male (TP) Leptoscarus vaigiensis, specimen ASM‐2015‐095, SL: 186 mm. (a, b, c) External mesial views of the premaxillaries. (a) 3D volume showing that only the fangs and the functional tip of the marginal dentition are anatomically apparent. (b) Maximum projection rendering providing in situ observation of the number of teeth and their arrangement within the marginal dentition. (c) Tracing of elements of interest along the rendered image in (a). White dotted lines show the parts of the image (a) that have been cropped. Taken together, (a) (b) and (c) show that only the functional part of the marginal dentition appears (in white), while the rest of this dentition is covered with a bony plate (in bright green). Supra‐marginal fangs (in orange and red) are implanted at the dorsal limit of the marginal dentition. The mesial supra‐marginal fangs (in orange) are graphically differentiated from the distal supra‐marginal fangs (in red). The enameloid cap of fangs is drawn in white and the dentine (dark orange and red) is differentiated from the attachment tissues (light orange and red). The black lines drawn on the surfaces of distal fangs correspond to the observable dentine folds. Surfaces colored in dark gray indicate scars from lost or broken teeth. (d) External lateral view of the distal supra‐marginal fangs borne by the left premaxilla. Only the left fang was visible on the frontal view as the right fang is erupting. As the erupting fang is not yet attached to the premaxilla, we were able to virtually extract it from its socket to display it in full on the image (e). (e) Ventral and mesial view of the virtually extracted fang showing the undulations of the outer surface of the dentine which become more pronounced toward the base of the tooth. Headlight symbols indicate the direction of view in the image whose letter is indicated in brackets. Scale bars are 2 mm for (a,b,c,d) and 500 μm for (e).

FIGURE 3

Organization of the premaxillary dentition in an adult male (TP) Calotomus carolinus, specimen ASM‐2014‐002, SL: 232 mm. (a, b) External mesial views of the premaxillaries. The large mesial marginal teeth (in blue) are distinguishable from the much smaller crowns of the distal marginal teeth, which are covered by a bony plate (in bright green). Two supra‐marginal fangs (in red) are present distally on each side of the upper jaw. Enameloid caps of teeth are drawn in white and the dentine (dark blue and red) is differentiated from the attachment tissues (light blue and red). The black lines drawn on the surface of distal fangs correspond to the observable dentine folds. Dark gray surfaces indicate abrasions or fractures on crowns of the mesial teeth. (c) External lateral view of the left premaxilla, which shows the robust and curved shape of the supra‐marginal fangs. White dotted lines show the parts of the image (a) that have been cropped. (d) Oblique, ventral view of the lower and upper dentition near occlusion. The black dotted circle shows that the lower marginal teeth abut against the dentinal shaft of the first left upper fang, which generates a notch (e) Ventral surface of the second upper left fang which shows numerous folds within the dentinal shaft. Headlight symbols indicate the direction of view in the image whose letter is indicated in brackets. Scale bars are 3 mm for (a, b, c, d) and 1 mm for (d, e).

FIGURE 4

Organization of the premaxillary dentition in an adult male (TP) Scarus psittacus, specimen AST‐2017‐048, SL: 290 mm. (a, b, c) External mesial views of the premaxillaries. (a) 3D volume showing that only the distal fangs and two rows of marginal teeth are visible. (b) Enlarged view on which the anatomical elements of interest have been schematized. (c) Maximum projection rendering allowing observation of the whole marginal dentition. Taken together, (a) (b) and (c) show that only the functional part of the marginal dentition appears (in white), while the rest of this dentition is covered by a bony plate (in bright green). A transverse row of supra‐marginal fangs (in red) is implanted at the distal limit of the marginal dentition. Enameloid caps of fangs are drawn in white and the dentine (dark red) is differentiated from the attachment tissues (light red). Dark gray surfaces indicate worn or broken fangs. (d, e) 3D volume and associated enlarged diagram of the external lateral view of the left premaxilla. (f, g) 3D volume and associated enlarged diagram of the external lateral view of the left dentary. White dotted lines in (b, e, g) show the parts of the associated images that have been cropped. Color codes for (e) and (g) are the same as for (b). Headlight symbols indicate the direction of view in the image whose letter is indicated in brackets. All scale bars are 2 mm.

FIGURE 5

Longitudinal sections of fangs of Calotomus carolinus (a), Leptoscarus vaigiensis (b) and Scarus psittacus (c). These sections show that fangs are shallowly implanted into the alveolar bone sockets. (a) Dentine folds become clearly apparent in the basal third of the inner dentinal wall and the pulp cavity is entirely free of mineralized tissue. (b) Two‐thirds of the inner dentinal wall shows marked dentinal folds and alveolar bone is (modestly) present within the pulp cavity. (c) The dentinal wall is very thick (the dentinal folds will only be visible on perpendicular sections) and a massive bony plug has invaded the pulp cavity. All scale bars are 700 μm.

FIGURE 6

Internal structure of mineralized tissues in the supra‐marginal and distal fangs. (a, b, c, d, e, f) Virtual horizontal slices through the basal parts of fangs illustrate the diversity of plicidentine patterns as well as the periodontal tissues along the fangs. (a, b, c, d) Sections of four different fangs of Leptoscarus vaigiensis, specimen ASM‐2015‐095. (a) Section of a newly emerged, not yet functional fang showing no contact between the plicidentine (bright green) and the edges of the socket made of jaw bone (light blue). The pulp cavity is free of any mineralized tissue (black circle bordered in white). (b) As the fangs become more mature, their outer dentinal wall first fuses with the jawbone via alveolar bone mineralization (red), while the pulp cavity remains free. At the periphery of the dentine layer is a white border that is consistent with cementum (fuchsia arrow). (c) Once the fang is attached externally, a second phase of alveolar bone mineralization (red) gradually invades the pulp cavity. (c) is an early stage and (d) is a late stage of alveolar bone mineralization of the pulp cavity. (e, f) Fangs of Calotomus carolinus, specimen ASM‐2014‐002, and Scarus psittacus, specimen AST‐2017‐048, respectively. (e) and (f) show a diversity of dentinal wall plication pattern in fangs that are both externally attached but still have a free pulp cavity. All scale bars are 500 μm.

FIGURE 7

Variation in dentine folding pattern in a fang of Leptoscarus vaigiensis, specimen ASM‐2015‐095. (a) The fang as seen from its tip perpendicular to the upper jaw. (b) Virtual longitudinal section of the fang. White dotted lines indicate the three virtual cutting planes studied and refer to the diagrams (c, d, e). In the diagrams (c, d, e, f, g, h), the internal and external walls of the dentine are drawn in red and white, respectively, while the dentine is colored in gray and the pulp cavity in black. (c, d, e) show that the number and wavelength of dentine folds change little toward the base of the tooth, while their amplitudes increase. (f, g, h) are cumulative views of the external contour (f), the internal contour (g), and the two contours of the dentine walls. The observation of (f) and (g) show that the complexity of the dentine plications is greater on the distal side of the tooth. d: distal, v: ventral. Scale bars for (a, b) are 500 μm.

FIGURE 8

Thin sections through the bases of two supra‐marginal fangs of a Leptoscarus vaigiensis, specimen ASM‐2015‐095. (a) Cross section of the premaxilla showing two supra‐marginal fangs in transverse section and the marginal dentition in the longitudinal plane. White circles edged in black: free pulp cavity, red dots: alveolar bone, bright green dots: secondary dentine, yellow dots: primary dentine, fuchsia arrows: cementum, light blue dots: jaw bone. Images (b) and (c) are focused on the areas of (a) which are indicated by white dotted rectangles. Scale bars are 500 μm for (a) and 50 μm for (b, c).

FIGURE 9

Closeup images of the attachment tissues along the base of a supra‐marginal fang of Leptoscarus vaigiensis in thin section. (a) Plane‐polarized light image of the attachment tissues. Note the fibrous texture of the alveolar bone (red dot) compared to the surrounding jawbone (light blue dot). (b) Cross‐polarized light image of the attachment tissues in (a) highlighting the band of acellular cementum (fuchsia dot) coating the dentine of the supra‐marginal fang. Scale bars are 50 μm.