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. 2020 Sep 15:8:e9771.
doi: 10.7717/peerj.9771. eCollection 2020.

Osteohistology and growth dynamics of the Brazilian noasaurid Vespersaurus paranaensis Langer et al., 2019 (Theropoda: Abelisauroidea)

Geovane Alves de Souza  1 , Marina Bento Soares  2 , Arthur Souza Brum  1 , Maria Zucolotto  3 , Juliana M Sayão  4 , Luiz Carlos Weinschütz  5 , Alexander W A Kellner  2
Affiliations

Osteohistology and growth dynamics of the Brazilian noasaurid Vespersaurus paranaensis Langer et al., 2019 (Theropoda: Abelisauroidea)

Geovane Alves de Souza et al. PeerJ. .

Abstract

Although the knowledge of bone histology of non-avian theropods has advanced considerably in recent decades, data about the bone tissue patterns, growth dynamics and ontogeny of some taxa such as abelisauroids are still limited. Here we describe the bone microstructure and growth dynamics of the Brazilian noasaurine Vespersaurus paranaensis using five femora and six tibiae and quantify the annual growth marks through retrocalculation of missing ones to estimate ontogenetic ages. The femoral series comprises four femoral histological classes (FHC I-IV), varying from two annuli or LAGs to seven LAGs. Femora show that sexual maturity was achieved around the seventh to tenth year of life, whereas the tibiae suggest it was earlier (around three to five years old). Tibiae represent three histological classes (THC I-III) displaying from three to nine LAGs. Two tibiae (THC III) exhibit an external fundamental system indicating that these specimens reached full skeletal size. The heterogeneous maturity observed in Vespersaurus hind limb bones could result from differential allometry scaling between femora and tibiae length with the body length. The predominant parallel-fibered bone matrix suggests that Vespersaurus grew more slowly than most theropods, including other abelisauroids, in a pattern shared with the noasaurines Masiakasaurus knopfleri from Madagascar and CPPLIP 1490 from Brazil. This deviation from the typical theropod growth pattern may be mainly correlated with small body size, but also may related to resource limitation imposed by the arid climate prevailing in southwestern Gondwana during Cretaceous. Moreover, given the ecological and phylogenetic similarities among these taxa, such features would probably be apomorphic within Noasauridae.

Keywords: Abelisauroidea; Brazil; Cretaceous; Dinosauria; Vespersaurus.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Cladogram of Abelisauroidea, comparing body length and primary bone tissue type of the histologically analyzed taxa.
Sizes in scale based on BL estimations of Grillo & Delcourt (2017). From the larger to the smaller: Aucasaurus garridoi (6.2 m), Quilmesaurus curriei (5.3 m), MMCh-PV 69 (4.2 m), ROM 64666 (2 m), Limusaurus inexplicabilis (1.7 m), Masiakasaurus knopfleri (1.8 m), Vespersaurus paranaensis (1.5 m) and CCLPP 1490 (1.4 m). Phylogenetic hypothesis based on Rauhut & Carrano (2016) and Langer et al. (2019). Branch lengths indicate distance from the plesiomorphic fibrolamellar pattern.
Figure 2
Figure 2. Hind limb bones of Vespersaurus paranaensis.
(A–E) Femora. (A) CP.V 4142 (left), in anterior view. (B) CP.V 2277 (left) in anterior view. (C) CP.V 4264 (left) in lateral view. (D) CP.V 4136 (left) in anterior view. (E) CP.V 4206 (left) in posterior view. (F–J) Tibiae. (F) CP.V 4140 (left) in lateral view. (G) CP.V 4130 (right) in medial view. (H) CP.V 4312a (left) in medial view. (I) CP.V 2385 (left) in anterior view. Red lines indicate the locations where the histological cross-sections were taken. Scale bar: 3 cm.
Figure 3
Figure 3. Femoral Histological Class (FHC) I of Vespersaurus paranaensis.
(A) Whole cross-section of CP.V 4136. (B) High magnification of the deep cortex showing microstructural pattern in CP.V 4136. (C) Cortex of CP.V 4136 showing two bands of poorly vascularized lamellar bone (white arrow) interpreted as annuli. (D) The same image in polarized light. Thin layer of endosteal lamella surrounding the medullary cavity is present in this region of the cross-section, evidenced by polarized light. Abbreviations: el, endosteal lamellae; mc, medullary cavity. Scale bars: 3 mm in (A), 100 μm in (B) and 1000 μm in (C).
Figure 4
Figure 4. Femoral Histological Class (FHC) II and III of Vespersaurus paranaensis.
(A–C) Whole cross-sections of femora CP.V 4142 (FHC II), CP.V 4206 (B; FHC II) and CP.V 4264 (FHC III), respectively. (D) Cortex of CP.V 4142. (E) Cortex of CP.V 4206 showing a large amount of secondary osteons and peripheral cortex poorly vascularized. (F) Cortex of CP.V4264 showing deep cortex with resorption cavities covered by endosteal lamellae. (G) High magnification of the femur CP.V 4264 showing a endosteal lamellae in detail. (H) Peripheral outer cortex showing primary osteons. (I) Cross-section of femur CP.V4264 showing double LAGs. White arrows indicate LAGs. Abbreviations: el, endosteal lamellae; mc, medullary cavity; po, primary osteon; sb, secondary bone. Scale bar: 3 mm in (A)–(C), 500 μm in (D)–(I), apart (G), which is equal to 80 μm.
Figure 5
Figure 5. Femoral Histological Class (FHC) IV of Vespersaurus paranaensis.
(A) Whole cross-section of CP.V 2277. (B) External and (C) internal cortex of CP.V 2277 showing the large amount of double and triple LAGs, and vascularization variation between zones (overlapping images). (D) Other cortical region of CP.V 2277 showing forked LAGs in normal and (E) polarized light. Note that specimen has no endosteal lamellae covering the medullary cavity. White arrows indicate LAGs. Abbreviation: mc, medullary cavity. Scale bar: 3 mm in (A) and 300 μm in (B)–(E).
Figure 6
Figure 6. Tibial Histological Class (THC) I of Vespersaurus paranaensis.
(A and B) Whole cross-sections of tibiae CP.V 4203 and CP.V 4312a, respectively. (C) Cortical zone detail of CP.V 4203. (D) Sub-periosteal cortex of CP.V 4203 under polarized light. (E) Cortical zone detail of CP.V 4312a. (F and G) Primary osteons and isolated secondary osteons of CP.V 4203. Note the diameter variation between vascular channels of the secondary osteons. (H) Detail of LAGs of CP.V 4312a under polarized light. White arrows indicate LAGs. Abbreviations: el, endosteal lamellae; LAG, line of arrested growth; mc, medullary cavity; po, primary osteon; sb, secondary bone, so, secondary osteon; t, trabeculae. Scale: 3 mm in (A) and (B), 300 μm in (C) and (E), 80 μm in (F) and (G) and 10 μm in (D) and (H).
Figure 7
Figure 7. Tibial Histological Class (THC) II of Vespersaurus paranaensis.
(A and B) Whole cross-section of tibiae CP.V 4140 and CP.V 4000, respectively. (C) High magnification of the cortex of CP.V 4140. (D) Endosteal drift in the deep cortex of CP.V 4140. (E) Large amount of Haversian (secondary) bone and close packed LAGs not forming EFS in CP.V 4140. (F) Trabecular bone with secondary osteons in perimedullary zone of the cortex in CP.V 4140. (G) High magnification of the cortex of CP.V 4000.The Haversian bone can occupy between 1/3 and 1/5 of the cortex (C and E). White arrows indicate LAGs. Abbreviations: el, endosteal lamellae; LAG, line of arrested growth; mc, in (A) and (B), 200 μm in (C), (E), (F) and (G) and 400 μm in (D). Medullary cavity; sb, secondary bone, so, secondary osteon; t, trabeculae. Scale: 3 mm.
Figure 8
Figure 8. Tibial Histological Class (THC) III of Vespersaurus paranaensis.
(A and B) Whole cross-section of tibiae CP.V 2385 and CP.V 4130, respectively. (C) Cortex of CP.V2385 showing the large and stratified endosteal lamellae. (D) Cortex of CP.V 4130 in panoramic view. (E) Variation of the vascular pattern from plexiformreticular to reticular in CP.V 4130. (F) Deep cortex of CP.V 4130 showing the bulk of secondary osteons between cortex and endosteal lamella in normal and (G) polarized light (see the small patch of woven bone). (H) Close packed LAGs within the EFS of CP.V 2385 in polarized light and (I) CP.V 4130 in normal light. White arrows indicate LAGs. Abbreviations: EFS, External fundamental system; el, endosteal lamellae; LAG, line of arrested growth; mc, medullary cavity; pb, primary bone; pvc, plexiform channels; rvc, reticular vascular channels; sb, secondary bone; wvb, woven bone. Scale bar: 3 mm in (A) and (B), 200 μm in (C)–(G), 50 μm in (H) and 100 μm in (I).
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