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. 2017 Feb 27;12(2):e0172781.
doi: 10.1371/journal.pone.0172781. eCollection 2017.

Squamation and ecology of thelodonts

Humberto G Ferrón  1 , Héctor Botella  1
Affiliations

Squamation and ecology of thelodonts

Humberto G Ferrón et al. PLoS One. .

Abstract

Thelodonts are an enigmatic group of Paleozoic jawless vertebrates that have been well studied from taxonomical, biostratigraphic and paleogeographic points of view, although our knowledge of their ecology and mode of life is still scant. Their bodies were covered by micrometric scales whose morphology, histology and the developmental process are extremely similar to those of extant sharks. Based on these similarities and on the well-recognized relationship between squamation and ecology in sharks, here we explore the ecological diversity and lifestyles of thelodonts. For this we use classic morphometrics and discriminant analysis to characterize the squamation patterns of a significant number of extant shark species whose ecology is well known. Multivariate analyses have defined a characteristic squamation pattern for each ecological group, thus establishing a comparative framework for inferring lifestyles in thelodonts. We then use this information to study the squamation of the currently described 147 species of thelodonts, known from both articulated and disarticulated remains. Discriminant analysis has allowed recognizing squamation patterns comparable to those of sharks and links them to specific ecological groups. Our results suggest a remarkable ecological diversity in thelodonts. A large number of them were probably demersal species inhabiting hard substrates, within caves and crevices in rocky environments or reefs, taking advantage of the flexibility provided by their micromeric squamations. Contrary to classical interpretations, only few thelodonts were placed among demersal species inhabiting sandy and muddy substrates. Schooling species with defensive scales against ectoparasites could be also abundant suggesting that social interactions and pressure of ectoparasites were present in vertebrates as early the Silurian. The presence of species showing scales suggestive of low to moderate speed and a lifestyle presumably associated with open water environments indicates adaptation of thelodonts to deep water habitats. Scale morphology suggests that some other thelodonts were strong-swimming pelagic species, most of them radiating during the Early Devonian in association with the Nekton Revolution.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Diagram illustrating the methodology used to quantify the body surface area covered by each scale morphotype in a model shark (Galeorhinus galeus).
(A) Representation of the different body areas on Cartesian coordinate systems. (B) Hypothetical body distribution of the scale morphotypes and their representation on the Cartesian coordinate systems (scale morphotypes covering negligible surfaces, such as the circum-oral region or the fin leading edges, have not been considered for the quantitative approach and are not shown on the graphs). Galeorhinus galeus drawing taken from Shark Trust [72], courtesy of Marc Dando. Scale drawings modified from Compagno [62]. Abbreviations: AF, anal fin; CF, caudal fin; DF 1, first dorsal fin; DF 2, second dorsal fin; DL, dorso-lateral region; PFd, dorsal surface of the pectoral fin; pFd, dorsal surface of the pelvic fin; PFv, ventral surface of the pectoral fin; pFv, ventral surface of the pelvic fin; V, ventral region.
Fig 2
Fig 2. Ecological parameters considered for all studied species of sharks arranged by the ecological groups defined by Reif [15].
Data were mainly taken from Reif [15], Compagno [62, 63, 64], Shark Trust [72], Compagno et al. [73], Froese and Pauly [74], Ebert et al. [75] and IUCN [76]. Reported bathymetric ranges are represented by black bars where usual bathymetric ranges are indicated with thickened portions on the right side of the diagram. All shark drawings taken from Shark Trust [72], courtesy of Marc Dando. Abbreviations: Habitat (CS, continental shelf; N, neritic zone; O, oceanic zone; oCS, outer continental shelf; S, slope; uS, upper slope), relative location to the seafloor (B, benthopelagic; D, demersal; P, pelagic), substrate preference (H, hard substrate; NR, not reported; S, soft substrate), frequency of schooling (H, high; L, low; NR, not reported).
Fig 3
Fig 3. Canonical Variate Analysis-1 (CVA-1) taking eight scale morphotypes (M1-M8, corresponding to five functional types) as defined groups (modified from Reif [15]) and ten size-free variables of the crown surface as discriminant variables.
Results are plotted based on the first two discriminant functions. (A) CVA-1 results of shark scales of known morphotype (original cases). (B) Classification results and discriminant punctuations of shark scales of unknown morphotype after their inclusion in CVA-1. (C) Classification results and discriminant punctuations of all studied thelodont scales after their inclusion in CVA-1 (note that all cases assigned to M.2, M.3 and M.5 come from disarticulated remains). Polygon outlines in B and C represent discriminant punctuations of original shark scales. (D) Comparison between discriminant punctuations of all shark scales (dashed polygon outlines) and all thelodont scales (filled polygons) arranged by morphotypes. Scale drawings modified from Compagno [62, 63, 64].
Fig 4
Fig 4. Canonical Variate Analysis-2 (CVA-2), six ecological groups of sharks taken as defined groups (modified from Reif [15]) and percentages of coverage of each scale morphotype used as discriminant variables.
Results are plotted based on the first two discriminant functions. All shark drawings taken from Shark Trust [72], courtesy of Marc Dando.
Fig 5
Fig 5. Characteristic squamation pattern of the seven ecological groups of sharks defined by Reif [15] showing the body distribution of scale morphotypes and functional types.
(A) Large near-shore hunters (illustrated by Carcharhinus brachyurus). (B) Fast pelagic hunting species (illustrated by Isurus oxyrinchus). (C) Schooling species of low to moderate speed (illustrated by Squalus acanthias). (D) Demersal species on rocky substrates and in caves (illustrated by Ginglymostoma cirratum). (E) Demersal species on sandy and muddy substrates (illustrated by Scyliorhinus canicula). (F) Mesopelagic luminescent species (illustrated by Etmopterus spinax). (G) Slow species of the open water (illustrated by Hexanchus griseus). All shark drawings taken from Shark Trust [72], courtesy of Marc Dando. Scale drawings modified from Compagno [62, 63, 64].
Fig 6
Fig 6. Distribution of scale functional types in articulated specimens of thelodonts, including complete and partial squamations and patches of scales.
(A) Archipelepis bifurcata (GSC 117 187) (B) Archipelepis turbinata (UALVP 32990). (C) Cometicercus talimaae (UALVP 33207). (D) Drepanolepis maerssae (UALVP 32917). (E) Eestilepis prominens (GSC 117 198). (F) Erepsilepis margaritifera (UALVP 43115). (G) Furcacauda fredholmae (reconstruction from several articulated remains) (H). Furcacauda heintzae (reconstruction from several articulated remains). (I) Lanarkia horrida (NMS.G.1991.48.3A). (J) Lanarkia horrida (NMS.G.1991.48.3B). (K) Lanarkia lanceolata, (NMS.G.1991.48.6). (L) Lanarkia spinulosa (GSE 5977). (M) Loganellia prolata (GSC 117 178). (N) Loganellia scotica (AM.F.89433A). (O) Loganellia scotica (AM.F.89433B). (P) Loganellia sulcata (UALVP 43150). (Q) Loganellia sulcata (GSC 117 177). (R) Nikolivia milesi (BMNH.P.53902). (S) Pezopallichthys ritchiei (reconstruction from several articulated remains). (T) Phillipsilepis cornuta (UALVP 43123). (U) Phillipsilepis crassa (GSC 117 182). (V) Phillipsilepis pusilla (GSC 117 186). (W) Phlebolepis elegans (reconstruction from several articulated remains). (X) Shielia gibba (GSC 117 181). (Y) Shielia parca (GSC 117 179). (Z) Shielia taiti (NMS.G.1991.48.7A). (A’) Shielia taiti (NMS.G.1991.48.7B). (B’) Sphenonectris turnerae (reconstruction from several articulated remains). (C’) Thelodus laevis (TUG 1025–1052). (D’) Thelodus macintoshi (MCZ 2035). (E’) Turinia pagei (NMS.G.1891.92.133). Specimens of Illoganellia colossea (UALVP 43129, GSC 117 199) and Thelodus inautditus (UALVP 43141) are not figured because the morphology of their patches is not defined in the literature. Anterior is left for all specimens. Scale bars, 1cm.
Fig 7
Fig 7. Phylogeny of sharks, with distribution of ecological groups and scale morphotypes.
More than 50 species are represented, including taxa studied here and some taxa examined by Reif [15] (denoted with asterisk). M5 is separated in two morhotypes (M5a and M5b) according to the distance betwen ridges (see Table 1 and text). Colours specify ecological assignation and numbers indicate major phylogenetic groups (1, Squalomorphii; 2, Galeomorphii; 3, Hexanchiformes; 4, Pristiophoriformes; 5, Squatiniformes; 6, Squaliformes; 7, Heterodontiformes; 8, Lamniformes; 9, Orectolobiformes; 10, Carcharhiniformes). Galeorhinus galeus is denoted with two different colors as the ecology of juveniles is different than that of the adults. Phylogenetic interrelationships are based on Vélez-Zuazo and Agnarsson [85].
Fig 8
Fig 8. Summary of the ecological diversity present in thelodonts including both CVA and qualitative assignments.
Bar charts show the absolute number and percentage of species assigned to each ecological group considering all species of thelodonts both together (A) and arranged by the currently described orders (B and C). Dashed rectangle outlines with question mark represent a number or a percentage of species whose assignment is uncertain. Uncertainties situated between two ecological groups correspond to species that belong to one of these two groups but a definitive assignment is not possible without further data. Uncertainties situated at the top of the bar represent species that could belong to any of the ecological groups. Drawings of Larolepis darbyi scales (Sandiviiformes?), Loganellia scotica (Loganelliiformes), Shielia taiti (Shieliiformes), Phlebolepis elegans (Phlebolepidiformes), Lanarkia horrida (Thelodontiformes), Furcacauda fredholmae (Furcacaudiformes), Longodus acicularis scales (Incertae sedis) and scales of Thulolepis striaspina (Incertae sedis) taken from Sansom and Elliott [93], Halstead and Turner [94], Märss and Ritchie [47], Ritchie [95], Turner [11], Wilson and Caldwell [58], Märss [92] and Blom [78] respectively.
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