Editorial Type:
Article Category: Research Article
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Online Publication Date: 16 Nov 2015

Functional and Developmental Morphology of Tooth Replacement in the Atlantic Wolffish, Anarhichas lupus (Teleostei: Zoarcoidei: Anarhichadidae)

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Page Range: 886 – 901
DOI: 10.1643/OT-14-141
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Adult Atlantic Wolffish, Anarhichas lupus, have a heterodont oral dentition consisting of long caniniform teeth in the symphysial regions of the dentaries and premaxillae and large molariform teeth posteriorly on the dentaries, dermopalatines, and vomer. Teeth are ankylosed to the bone of attachment. Wolffish use the caniniform teeth to capture prey including molluscs, crustaceans, echinoderms, and, less commonly, fishes. Prey are transported posteriorly and crushed between the molariform teeth. The molariform teeth of adults fit closely together despite individually variable shapes and sizes in a space-filling pattern that we term anamestic. Adult wolffish have an unusual tooth replacement pattern in which teeth are lost and subsequently replaced all at once, a pattern called simultaneous replacement. We used dissection, osteology, histology, and micro-computed tomography (CT) to study tooth replacement in a series of Anarhichas lupus from the western North Atlantic. Tooth development is intraosseous, with new tooth germs eroding into a specialized spongy portion of the bone of attachment. Simultaneous replacement involves extensive remodeling of this spongy bone. As planktonic larvae, wolffish have uniformly conical teeth, but relatively soon after settling a heterodont dentition similar to that of adults begins to develop. Juveniles exhibit a striking left-right symmetry of oral teeth and lack the anamestic pattern seen in adults. We compare tooth replacement in Atlantic Wolffish with that of Bluefish, Pomatomus saltatrix, another teleost with intraosseus tooth replacement. Patterns of intraosseous replacement in these taxa represent different evolutionary solutions to different ecological conditions, particularly diets. Not all teleosts with intraosseous tooth development are heterodont, but we predict that teleosts with heterodont dentitions will have intraosseous tooth development because this offers a way to provide attachment for functional teeth while replacement teeth are developing.

Copyright: © 2015 by the American Society of Ichthyologists and Herpetologists
Fig. 1. 
Fig. 1. 

Oral teeth of a large adult Anarhichas lupus and an excerpt of its description, reproduced from Andre (1784:277, table XI). Text included here is from the original publication and preserves typographical conventions of the 18th century. Structures indicated in the original drawing are: (A) vomer, (B) dermopalatines, (C) premaxillae, and (D) dentaries. Note that there are three rows of molariform teeth on the right dentary; teeth are missing from some tooth loci in the left dentary, but it, too, has three rows of teeth.

Fig. 2. 
Fig. 2. 

Frames from a video of wolffish feeding. Original video recording by Jonathan Bird. Used with permission.

Fig. 3. 
Fig. 3. 

Head and dentition of adult wolffish, anterior to left. (A) Lateral view to show lips and caniniform teeth (CU 97489A). (B) Palatal view to show arrangement of dentition and soft tissues (CU 97489B). (C) View of lower jaw to show arrangement of dentition and soft tissues. Arrows indicate the narrow portion of lower jaw (CU 97489B). (D) Lateral view of skull (CU 97490). (E) Bones and teeth of upper jaw and palate. Red asterisks indicate loci from which teeth were lost during preparation (CU 97490). (F) Bones and teeth of lower jaw. Arrows indicate the narrow portion of lower jaw. Boxed area indicates the pulpit of the left dentary (CU 97490).

Fig. 4. 
Fig. 4. 

Right lateral view of articulated upper and lower teeth showing pulpit of lower jaw (CU 97490).

Fig. 5. 
Fig. 5. 

Isolated caniniform and molariform teeth of an adult wolffish (CU 95992). (A) Lateral view of crown of a caniniform tooth from the dentary. (B) Basal view of tooth in A. (C) Lateral view of crown of molariform tooth of dentary. (D) Basal view of tooth in C.

Fig. 6. 
Fig. 6. 

Micro-CT scan of dentary teeth and bone of attachment to show density of tissues viewed anteriorly (CU 95999). Yellow colors indicate denser tissues; purple indicates less dense tissues.

Fig. 7. 
Fig. 7. 

Transverse thick epoxy section of anterior portion of dentary to show relationships of teeth, spongy bone, lamellar bone, and associated soft tissues (CU 97489B). Labial to right side. Asterisks indicate canals in the osteodentine. Section thickness 200 µm; unstained.

Fig. 8. 
Fig. 8. 

Dissection of right upper lip and premaxilla to show position of replacement pores and developing tooth germs (CU 98017). (A) View of partially prepared specimen with lip intact. (B) Lip reflected to show developing tooth germs and replacements pores.

Fig. 9. 
Fig. 9. 

Shaded digital 3D model from micro-CT data set to show an early stage in the appearance of replacement pores and tooth germs (red arrows) adjacent to the teeth they will replace (CU 97638). (A) Labial surface of left lower jaw. (B) Lingual surface of left lower jaw.

Fig. 10. 
Fig. 10. 

Transverse thick epoxy section of anterior portion of dentary to show tooth germ in replacement pore (CU 97489B). Labial to right side. (A) Caniniform tooth germ with dental lamina continuous with epithelial tissue of the gum. (B) Close up to show early formation of osteodentine tubules, dental organ, and blood vessels of the soft pulp. Section thickness <100 µm; unstained.

Fig. 11. 
Fig. 11. 

Digitally reconstructed 2D view from micro-CT data set to show late stage in the formation of replacement teeth in the dentary, dermopalatine, and premaxilla (CU 96316). Anterior to left. All developing teeth are surrounded by spongy bone.

Fig. 12. 
Fig. 12. 

Developing replacement molariform teeth of left dentary to show red-tooth stage in tooth replacement cycle (CU 96317). Anterior to left.

Fig. 13. 
Fig. 13. 

Transverse LVN section of anterior portion of left premaxilla of a specimen in the red-tooth stage in tooth replacement cycle (CU 96317). Labial to left. At one locus, the tooth has already been lost; at the adjacent locus, the tooth is in the process of being lost. Two replacement teeth are developing surrounded by spongy bone. Section thickness 60 µm; stained with hematoxylin and picro-ponceau. Same specimen as shown in Figure 12.

Fig. 14. 
Fig. 14. 

Micro-CT scans of a pelagic larva, Anarhichas sp., 27.52 mm TL (MCZ 169188). (A) Anterior view to show teeth of vomer, premaxilla, and dentary bones. (B) Digitally dissected and isolated lower jaw to show ankylosed and developing teeth. Stained with iodine.

Fig. 15. 
Fig. 15. 

Dentition in a cleared-and-stained wolffish, 49.5 mm TL, a newly settled juvenile (CU 98016). Anterior to left.

Fig. 16. 
Fig. 16. 

Micro-CT scans of a juvenile wolffish, 91.2 mm TL, collected in October 2008 (CU 98018). Anterior to left. (A) Lateral view of head. (B) Digitally dissected and isolated dentary to show ankylosed teeth, replacement teeth, and new teeth. (C) Digitally dissected and isolated bones of the upper jaw and palate to show ankylosed and new molariform teeth.

Fig. 17. 
Fig. 17. 

Oral teeth of wolffish form a W-shaped mill for crushing prey. Viewed from anterior.

Fig. 18. 
Fig. 18. 

Schematic diagrams showing two general modes of tooth replacement in teleosts. (A) Formation of new tooth germ. (B) Extraosseous tooth replacement showing a stage in which the tooth germ lies adjacent to the bone of attachment. (C) Intraosseous tooth replacement showing a stage in which the tooth germ has already eroded into the bone of attachment via a replacement pore.

Contributor Notes

Associate Editor: G. Arratia.

Received: 10 Sept 2014
Accepted: 10 Feb 2015
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