Quantitative histological models suggest endothermy in plesiosaurs

Abstract

Background: Plesiosaurs are marine reptiles that arose in the Late Triassic and survived to the Late Cretaceous. They have a unique and uniform bauplan and are known for their very long neck and hydrofoil-like flippers. Plesiosaurs are among the most successful vertebrate clades in Earth's history. Based on bone mass decrease and cosmopolitan distribution, both of which affect lifestyle, indications of parental care, and oxygen isotope analyses, evidence for endothermy in plesiosaurs has accumulated. Recent bone histological investigations also provide evidence of fast growth and elevated metabolic rates. However, quantitative estimations of metabolic rates and bone growth rates in plesiosaurs have not been attempted before.

Methods: Phylogenetic eigenvector maps is a method for estimating trait values from a predictor variable while taking into account phylogenetic relationships. As predictor variable, this study employs vascular density, measured in bone histological sections of fossil eosauropterygians and extant comparative taxa. We quantified vascular density as primary osteon density, thus, the proportion of vascular area (including lamellar infillings of primary osteons) to total bone area. Our response variables are bone growth rate (expressed as local bone apposition rate) and resting metabolic rate (RMR).

Results: Our models reveal bone growth rates and RMRs for plesiosaurs that are in the range of birds, suggesting that plesiosaurs were endotherm. Even for basal eosauropterygians we estimate values in the range of mammals or higher.

Discussion: Our models are influenced by the availability of comparative data, which are lacking for large marine amniotes, potentially skewing our results. However, our statistically robust inference of fast growth and fast metabolism is in accordance with other evidence for plesiosaurian endothermy. Endothermy may explain the success of plesiosaurs consisting in their survival of the end-Triassic extinction event and their global radiation and dispersal.

Keywords: Bone growth rate; Bone histology; Endothermy; Marine reptile; Metabolism; Phylogenetic comparative methods; Phylogenetic eigenvector maps; Plesiosauria; Vascular density.

Figure 1. Phylogenetic relationships, divergence times, and ages of the eosauropterygians investigated in this study.

The information is taken from Rieppel (2000), Ketchum & Benson (2010), and Wintrich et al. (2017). Divergence times (in Ma) are indicated at the nodes, and tip ages (in Ma) are indicated below the genus names.

Figure 2. Measuring primary osteon density exemplified for Plesiosaurus dolichodirus.

Primary osteon density is measured as the (pink circled) area of the vascular canals with the infillings by lamellar bone (primary osteons) compared to total bone area. Photo by Corinna Fleischle.

Figure 3. Measured and estimated mass-specific resting metabolic rate (RMR) with 95% confidence intervals.

Blue boxes indicate ectothermic species, red boxes indicate (possibly) endothermic species. All sauropterygians in the model have a RMR higher than the analyzed ectothermic species. For plesiosaurs, a RMR in the range of birds was even estimated.

Figure 4. Measured and estimated mass-specific resting metabolic rate (RMR) in log mL O₂ h⁻¹ g^−0.67 mapped color-coded on a phylogenetic tree.

In this comparison, blue represents low values, green and yellow intermediate values and red high values. Plesiosaurs have a RMR in the range of birds. Within sauropterygians, the RMR increases, but even basal forms show values in the range of mammals or higher and far above the ectothermic species included in the model.

Figure 5. Measured and estimated bone apposition rate with 95% confidence intervals.

Blue boxes indicate ectothermic species, red boxes indicate (possibly) endothermic species. All sauropterygians show a growth rate higher than the analyzed ectothermic species. Plesiosaurs have values in the range of birds.

Figure 6. Measured and estimated bone apposition rate in log μm/day mapped color-coded on a phylogenetic tree.

In this comparison, blue represents low values, green and yellow intermediate values and red high values. Plesiosaurs have a growth rate in the range of birds. Within sauropterygians, growth rate increases, but even basal forms show values in the range of mammals or higher and far above the ectothermic species included in the model.