Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)
Crushing and eating hard prey (durophagy) is mechanically demanding. The cartilage jaws of durophagous stingrays are known to be reinforced relative to non-durophagous relatives, with a thickened external cortex of mineralized blocks (tesserae), reinforcing struts inside the jaw (trabeculae), and pa...
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| Format: | Article |
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2022.932341/full |
| _version_ | 1811239126187376640 |
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| author | Brett Clark Júlia Chaumel Zerina Johanson Charlie Underwood Charlie Underwood Moya M. Smith Mason N. Dean Mason N. Dean |
| author_facet | Brett Clark Júlia Chaumel Zerina Johanson Charlie Underwood Charlie Underwood Moya M. Smith Mason N. Dean Mason N. Dean |
| author_sort | Brett Clark |
| collection | DOAJ |
| description | Crushing and eating hard prey (durophagy) is mechanically demanding. The cartilage jaws of durophagous stingrays are known to be reinforced relative to non-durophagous relatives, with a thickened external cortex of mineralized blocks (tesserae), reinforcing struts inside the jaw (trabeculae), and pavement-like dentition. These strategies for skeletal strengthening against durophagy, however, are largely understood only from myliobatiform stingrays, although a hard prey diet has evolved multiple times in batoid fishes (rays, skates, guitarfishes). We perform a quantitative analysis of micro-CT data, describing jaw strengthening mechanisms in Rhina ancylostoma (Bowmouth Guitarfish) and Rhynchobatus australiae (White-spotted Wedgefish), durophagous members of the Rhinopristiformes, the sister taxon to Myliobatiformes. Both species possess trabeculae, more numerous and densely packed in Rhina, albeit simpler structurally than those in stingrays like Aetobatus and Rhinoptera. Rhina and Rhynchobatus exhibit impressively thickened jaw cortices, often involving >10 tesseral layers, most pronounced in regions where dentition is thickest, particularly in Rhynchobatus. Age series of both species illustrate that tesserae increase in size during growth, with enlarged and irregular tesserae associated with the jaws’ oral surface in larger (older) individuals of both species, perhaps a feature of ageing. Unlike the flattened teeth of durophagous myliobatiform stingrays, both rhinopristiform species have oddly undulating dentitions, comprised of pebble-like teeth interlocked to form compound “meta-teeth” (large spheroidal structures involving multiple teeth). This is particularly striking in Rhina, where the upper/lower occlusal surfaces are mirrored undulations, fitting together like rounded woodworking finger-joints. Trabeculae were previously thought to have arisen twice independently in Batoidea; our results show they are more widespread among batoid groups than previously appreciated, albeit apparently absent in the phylogenetically basal Rajiformes. Comparisons with several other durophagous and non-durophagous species illustrate that batoid skeletal reinforcement architectures are modular: trabeculae can be variously oriented and are dominant in some species (e.g. Rhina, Aetobatus), whereas cortical thickening is more significant in others (e.g. Rhynchobatus), or both reinforcing features can be lacking (e.g. Raja, Urobatis). We discuss interactions and implications of character states, framing a classification scheme for exploring cartilage structure evolution in the cartilaginous fishes. |
| first_indexed | 2024-04-12T12:54:22Z |
| format | Article |
| id | doaj.art-0622c0cd88da4db59693859e1b6c405d |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-04-12T12:54:22Z |
| publishDate | 2022-10-01 |
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| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-0622c0cd88da4db59693859e1b6c405d2022-12-22T03:32:22ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-10-011010.3389/fcell.2022.932341932341Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)Brett Clark0Júlia Chaumel1Zerina Johanson2Charlie Underwood3Charlie Underwood4Moya M. Smith5Mason N. Dean6Mason N. Dean7Image and Analysis Centre, Core Research Labs, London, United KingdomDepartment of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam, GermanyNatural History Museum, London, United KingdomNatural History Museum, London, United KingdomDepartment of Earth and Planetary Sciences, Birkbeck, University of London, London, United KingdomCentre for Craniofacial and Regenerative Biology, Dental Institute, King’s College, London, United KingdomDepartment of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam, GermanyDepartment of Infectious Diseases and Public Health, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, ChinaCrushing and eating hard prey (durophagy) is mechanically demanding. The cartilage jaws of durophagous stingrays are known to be reinforced relative to non-durophagous relatives, with a thickened external cortex of mineralized blocks (tesserae), reinforcing struts inside the jaw (trabeculae), and pavement-like dentition. These strategies for skeletal strengthening against durophagy, however, are largely understood only from myliobatiform stingrays, although a hard prey diet has evolved multiple times in batoid fishes (rays, skates, guitarfishes). We perform a quantitative analysis of micro-CT data, describing jaw strengthening mechanisms in Rhina ancylostoma (Bowmouth Guitarfish) and Rhynchobatus australiae (White-spotted Wedgefish), durophagous members of the Rhinopristiformes, the sister taxon to Myliobatiformes. Both species possess trabeculae, more numerous and densely packed in Rhina, albeit simpler structurally than those in stingrays like Aetobatus and Rhinoptera. Rhina and Rhynchobatus exhibit impressively thickened jaw cortices, often involving >10 tesseral layers, most pronounced in regions where dentition is thickest, particularly in Rhynchobatus. Age series of both species illustrate that tesserae increase in size during growth, with enlarged and irregular tesserae associated with the jaws’ oral surface in larger (older) individuals of both species, perhaps a feature of ageing. Unlike the flattened teeth of durophagous myliobatiform stingrays, both rhinopristiform species have oddly undulating dentitions, comprised of pebble-like teeth interlocked to form compound “meta-teeth” (large spheroidal structures involving multiple teeth). This is particularly striking in Rhina, where the upper/lower occlusal surfaces are mirrored undulations, fitting together like rounded woodworking finger-joints. Trabeculae were previously thought to have arisen twice independently in Batoidea; our results show they are more widespread among batoid groups than previously appreciated, albeit apparently absent in the phylogenetically basal Rajiformes. Comparisons with several other durophagous and non-durophagous species illustrate that batoid skeletal reinforcement architectures are modular: trabeculae can be variously oriented and are dominant in some species (e.g. Rhina, Aetobatus), whereas cortical thickening is more significant in others (e.g. Rhynchobatus), or both reinforcing features can be lacking (e.g. Raja, Urobatis). We discuss interactions and implications of character states, framing a classification scheme for exploring cartilage structure evolution in the cartilaginous fishes.https://www.frontiersin.org/articles/10.3389/fcell.2022.932341/fullBatoideadurophagyjawtrabeculaetesseraetessellated cartilage |
| spellingShingle | Brett Clark Júlia Chaumel Zerina Johanson Charlie Underwood Charlie Underwood Moya M. Smith Mason N. Dean Mason N. Dean Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates) Frontiers in Cell and Developmental Biology Batoidea durophagy jaw trabeculae tesserae tessellated cartilage |
| title | Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates) |
| title_full | Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates) |
| title_fullStr | Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates) |
| title_full_unstemmed | Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates) |
| title_short | Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates) |
| title_sort | bricks trusses and superstructures strategies for skeletal reinforcement in batoid fishes rays and skates |
| topic | Batoidea durophagy jaw trabeculae tesserae tessellated cartilage |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2022.932341/full |
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