Determination of muscle strength and function in plesiosaur limbs: finite element structural analyses of Cryptoclidus eurymerus humerus and femur

Abstract

Background The Plesiosauria (Sauropterygia) are secondary marine diapsids. They are the only tetrapods to have evolved hydrofoil fore- and hindflippers. Once this specialization of locomotion had evolved, it remained essentially unchanged for 135 Ma. It is still controversial whether plesiosaurs flew underwater, rowed, or used a mixture of the two modes of locomotion. The long bones of Tetrapoda are functionally loaded by torsion, bending, compression, and tension during locomotion. Superposition of load cases shows that the bones are loaded mainly by compressive stresses. Therefore, it is possible to use finite element structure analysis (FESA) as a test environment for loading hypotheses. These include muscle reconstructions and muscle lines of action (LOA) when the goal is to obtain a homogeneous compressive stress distribution and to minimize bending in the model. Myological reconstruction revealed a muscle-powered flipper twisting mechanism. The flippers of plesiosaurs were twisted along the flipper length axis by extensors and flexors that originated from the humerus and femur as well as further distal locations. Methods To investigate locomotion in plesiosaurs, the humerus and femur of a mounted skeleton of Cryptoclidus eurymerus (Middle Jurassic Oxford Clay Formation from Britain) were analyzed using FE methods based on the concept of optimization of loading by compression. After limb muscle reconstructions including the flipper twisting muscles, LOA were derived for all humerus and femur muscles of Cryptoclidus by stretching cords along casts of the fore- and hindflippers of the mounted skeleton. LOA and muscle attachments were added to meshed volumetric models of the humerus and femur derived from micro-CT scans. Muscle forces were approximated by stochastic iteration and the compressive stress distribution for the two load cases, “downstroke” and “upstroke”, for each bone were calculated by aiming at a homogeneous compressive stress distribution. Results Humeral and femoral depressors and retractors, which drive underwater flight rather than rowing, were found to exert higher muscle forces than the elevators and protractors. Furthermore, extensors and flexors exert high muscle forces compared to Cheloniidae. This confirms a convergently evolved myological mechanism of flipper twisting in plesiosaurs and complements hydrodynamic studies that showed flipper twisting is critical for efficient plesiosaur underwater flight.

Deep‐time invention and hydrodynamic convergences through amniote flipper evolution

“…A flipper twisting mechanism was found to be necessary for underwater flight in plesiosaurs (Krahl et al, 2022; Krahl & Witzel, 2021) that involves the extensors and flexors that originate from the humerus and further distal flipper bones. A flipper twisting mechanism was found to be necessary for morphological and hydrodynamical reasons (Krahl, 2021; Krahl & Witzel, 2021) and for a physiological functional loading of the humerus (Krahl et al, 2022). The mechanism comprises muscular and ligamentous elements.…”

“…An active myological flipper twisting mechanism as well as muscles for flipper profile manipulation are well‐substantiated by the extant phylogenetic bracket consisting of Crocodilia and Lepidosauria (amended by Testudines) (Krahl & Witzel, 2021). Further support in favor of active flipper twisting in Cryptoclidus eurymerus was provided by finite element analyses of humerus and femur (Krahl et al 2022). In extant vertebrates that rely on lift‐based propulsion, flipper twisting plays a vital part in locomotion (Davenport, 1987; Walker & Westneat, 2000, 2002), but has rarely been research focus, too.…”

“…Plesiosaurs are Sauropterygia which are Mesozoic marine diapsids of uncertain phylogenetic origin (Merck, 1997; Neenan et al, 2013; Rieppel & Reisz, 1999) and have evolved a peculiar locomotory apparatus that includes hydrofoil fore‐ and hindflipper pairs that are looking almost identical (see Krahl, 2021 for review). As a consequence, scientists debated on how these four wing‐like flippers in plesiosaurs were used for locomotion (Araújo et al, 2015; Araújo & Correia, 2015; Carpenter et al, 2010; Frey & Riess, 1982; Godfrey, 1984; Halstead, 1989; Krahl, 2021; Krahl, Lipphaus, et al, 2022; Krahl & Witzel, 2021; Lingham‐Soliar, 2000; Liu et al, 2015; Long et al, 2006; Muscutt et al, 2017; Robinson, 1975, 1977; Tarlo, 1958; Tarsitano & Riess, 1982; Watson, 1924; Williston, 1914). Four different locomotory styles have been proposed for plesiosaurs: rowing (Araújo et al, 2015; Araújo & Correia, 2015; Tarlo, 1958; Watson, 1924; Williston, 1914), combinations of rowing and underwater flight phases with a shorter underwater flight phase like in the pig‐nosed turtle Carettochelys insculpta (Krahl, 2021; Figure 1c) or a longer underwater flight phase like in sea lions (Godfrey, 1984; Lingham‐Soliar, 2000; Liu et al, 2015; Figure 1e), and underwater flight like in sea turtles and penguins (Carpenter et al, 2010; Lingham‐Soliar, 2000; Liu et al, 2015; Krahl, 2021; Krahl & Witzel, 2021; Krahl, Lipphaus, et al, 2022; Muscutt et al, 2017; Robinson, 1975, 1977; Figure 1b,d).…”

“…As a consequence, scientists debated on how these four wing‐like flippers in plesiosaurs were used for locomotion (Araújo et al, 2015; Araújo & Correia, 2015; Carpenter et al, 2010; Frey & Riess, 1982; Godfrey, 1984; Halstead, 1989; Krahl, 2021; Krahl, Lipphaus, et al, 2022; Krahl & Witzel, 2021; Lingham‐Soliar, 2000; Liu et al, 2015; Long et al, 2006; Muscutt et al, 2017; Robinson, 1975, 1977; Tarlo, 1958; Tarsitano & Riess, 1982; Watson, 1924; Williston, 1914). Four different locomotory styles have been proposed for plesiosaurs: rowing (Araújo et al, 2015; Araújo & Correia, 2015; Tarlo, 1958; Watson, 1924; Williston, 1914), combinations of rowing and underwater flight phases with a shorter underwater flight phase like in the pig‐nosed turtle Carettochelys insculpta (Krahl, 2021; Figure 1c) or a longer underwater flight phase like in sea lions (Godfrey, 1984; Lingham‐Soliar, 2000; Liu et al, 2015; Figure 1e), and underwater flight like in sea turtles and penguins (Carpenter et al, 2010; Lingham‐Soliar, 2000; Liu et al, 2015; Krahl, 2021; Krahl & Witzel, 2021; Krahl, Lipphaus, et al, 2022; Muscutt et al, 2017; Robinson, 1975, 1977; Figure 1b,d).…”