Locomotory behaviour of early tetrapods from Blue Beach, Nova Scotia, revealed by novel microanatomical analysis

Abstract

Evidence for terrestriality in early tetrapods is fundamentally contradictory. Fossil trackways attributed to early terrestrial tetrapods long predate the first body fossils from the Late Devonian. However, the Devonian body fossils demonstrate an obligatorily aquatic lifestyle. Complicating our understanding of the transition from water to land is a pronounced gap in the fossil record between the aquatic Devonian taxa and presumably terrestrial tetrapods from the later Early Carboniferous. Recent work suggests that an obligatorily aquatic habit persists much higher in the tetrapod tree than previously recognized. Here, we present independent microanatomical data of locomotor capability from the earliest Carboniferous of Blue Beach, Nova Scotia. The site preserves limb bones from taxa representative of Late Devonian to mid-Carboniferous faunas as well as a rich trackway record. Given that bone remodels in response to functional stresses including gravity and ground reaction forces, we analysed both the midshaft compactness profiles and trabecular anisotropy, the latter using a new whole bone approach. Our findings suggest that early tetrapods retained an aquatic lifestyle despite varied limb morphologies, prior to their emergence onto land. These results suggest that trackways attributed to early tetrapods be closely scrutinized for additional information regarding their creation conditions, and demand an expansion of sampling to better identify the first terrestrial tetrapods.

Tetrapod terrestrialisation: a weight-bearing potential already present in the humerus of the stem-tetrapod fishEusthenopteron foordi

“…2.35 kg) -proportionally reflect the load imposed by the body weight of a stem tetrapod like Titktaalik on their humeri (with a humerus length = 7cm, (19); estimated body mass = 7 kg, (3)). This suggests that the numerous tubular marrow processes running longitudinally within the extended spongiosa in the limb bones of stem tetrapods (e.g., (11,16,17,46)) may have been key skeletal components to develop terrestrial locomotion rather than an obstacle to weight bearing, as previously thought (5,6,11). Of course, this trabecular configuration has a weight limit and this probably is a contributing factor for the humerus (and other long bones) to evolve into elongated bones with a narrow diaphysis, a thicker cortex and a drastically different morphology to ease terrestrial motion in larger tetrapods (5,57).…”

“…Surprisingly, none of them has considered the microanatomical architecture of the pectoral elements of stem tetrapods in their simulations although they are known to be very spongy. Microanatomical investigations conducted by several authors (6,11,12) concluded that the great sponginess of these elements was probably mechanically too weak to enable body weight support on land and this became commonly accepted (e.g., (5)).…”

“…Despite the high interest of the biology community for this crucial evolutionary event, it has been a challenge to date and characterise the terrestrial locomotory behavior of early tetrapods. In the last decades, the development of state-of-the-art biomechanical techniques/simulations (1)(2)(3)(4)(5)(6) and the discovery of new tetrapod trackways (7)(8)(9) has relaunched this interest. This started with the publication of Niedzwiedzki et al (7) proposing an origin for tetrapods deeper than previously suggested, into the early Middle Devonian.…”

“…Microanatomical investigations conducted by several authors (6,11,12) concluded that the great sponginess of these elements was probably mechanically too weak to enable body weight support on land and this became commonly accepted (e.g., (5)).…”

To be or not to be heavier: The role of dermal bones in the buoyancy of the Late Triassic temnospondyl amphibian Metoposaurus krasiejowensis

“…Most research on previously mentioned aquatic bone adaptations (osteosclerosis, osteoporotic‐like pattern, BMI or BMD, pachyostosis, and pachyosteosclerosis) are based on the long bones of amniotes (Amson et al, 2014; Canoville & Laurin, 2010; Canoville et al, 2016; Cooper et al, 2012; De Buffrénil et al, 1990, 2010; Gray et al, 2007; Houssaye, 2009, 2013, 2014a, 2015, 2016; Hugi et al, 2011; Kolb et al, 2011; Kriloff et al, 2008; Quemeneur et al, 2013; Sanchez et al, 2010). Furthermore, only a few studies have been conducted on the aquatic bone adaptations in anamniote taxa at the microanatomical level (Canoville & Chinsamy, 2015; Lennie et al, 2021; Mukherjee et al, 2010; Sanchez et al, 2010; Steyer et al, 2004). Mukherjee et al (2010) sheds light on the terrestrial lifestyle of trematosaurid temnospondyls from India, using description of local microanatomical variation.…”