Mammalian bone palaeohistology: a survey and new data with emphasis on island forms.

Christian Kolb,Analia M. Forasiepi,Shoji Hayashi,Lars W. Van den Hoek Ostende,Alexandra A.E. Van der Geer,Torsten M. Scheyer,Kristof Veitschegger,Eli Amson,Marcelo R. Sánchez-Villagra

doi:10.7717/peerj.1358

Christian Kolb, Analia M. Forasiepi + Show 7 more

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https://doi.org/10.7717/peerj.1358

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Abstract

The interest in mammalian palaeohistology has increased dramatically in the last two decades. Starting in 1849 via descriptive approaches, it has been demonstrated that bone tissue and vascularisation types correlate with several biological variables such as ontogenetic stage, growth rate, and ecology. Mammalian bone displays a large variety of bone tissues and vascularisation patterns reaching from lamellar or parallel-fibred to fibrolamellar or woven-fibred bone, depending on taxon and individual age. Here we systematically review the knowledge and methods on cynodont and mammalian bone microstructure as well as palaeohistology and discuss potential future research fields and techniques. We present new data on the bone microstructure of two extant marsupial species and of several extinct continental and island placental mammals. Extant marsupials display mainly parallel-fibred primary bone with radial and oblique but mainly longitudinal vascular canals. Three juvenile specimens of the dwarf island hippopotamid Hippopotamus minor from the Late Pleistocene of Cyprus show reticular to plexiform fibrolamellar bone. The island murid Mikrotia magna from the Late Miocene of Gargano, Italy displays parallel-fibred primary bone with reticular vascularisation and strong remodelling in the middle part of the cortex. Leithia sp., the dormouse from the Pleistocene of Sicily, is characterised by a primary bone cortex consisting of lamellar bone and a high amount of compact coarse cancellous bone. The bone cortex of the fossil continental lagomorph Prolagus oeningensis and three fossil species of insular Prolagus displays mainly parallel-fibred primary bone and reticular, radial as well as longitudinal vascularisation. Typical for large mammals, secondary bone in the giant rhinocerotoid Paraceratherium sp. from the Late Oligocene of Turkey is represented by dense Haversian bone. The skeletochronological features of Sinomegaceros yabei, a large-sized deer from the Pleistocene of Japan closely related to Megaloceros, indicate a high growth rate. These examples and the synthesis of existing data show the potential of bone microstructure to reveal essential information on life history evolution. The bone tissue and the skeletochronological data of the sampled island species suggest the presence of various modes of bone histological modification and mammalian life history evolution on islands to depend on factors of island evolution such as island size, distance from mainland, climate, phylogeny, and time of evolution.

Highlights

Histology of fossil bones (e.g., Ricqles, 1976a; Padian, 2011) provides data to investigate life history variables such as age, sexual maturity, growth patterns, and reproductive cycles
Characteristics of bone histology of the following taxa are either poorly or not at all documented in the literature (Table 1): the extant white-eared opossum Didelphis albiventris and the thick-tailed opossum Lutreolina crassicautada, the giant deer Megaloceros giganteus from the Late Pleistocene of Ireland, the Asian giant deer Sinomegaceros yabei from the Late Pleistocene of Japan, the extant southern pudu Pudu puda, the Cyprus dwarf hippopotamid Hippopotamus minor from the Late Pleistocene of Cyprus, the dormouse Leithia sp. from the Pleistocene of Sicily, the giant hornless rhinocerotoid Paraceratherium sp. from the Late Oligocene of Turkey, the continental pika Prolagus oeningensis from the Middle Miocene of La Grive, France, and the Sardinian pika Prolagus sardus from the Late Pleistocene
Three juvenile specimens of the dwarf island hippopotamid Hippopotamus minor from the Late Pleistocene of Cyprus show reticular to plexiform fibrolamellar bone, which does not indicate an island-specific pattern of bone growth or life history but a mode of growth similar to continental artiodactyl relatives instead

Summary

Introduction

Histology of fossil bones (e.g., Ricqles, 1976a; Padian, 2011) provides data to investigate life history variables such as age, sexual maturity, growth patterns, and reproductive cycles. The study of the microstructure of highly mineralised components such as blood vessel arrangement (De Boef & Larsson, 2007) and tissue types in bones as well as teeth (e.g., Kolb et al, 2015) provides information on growth patterns and remodelling processes of hard tissues in extinct vertebrates (see Scheyer, Klein & Sander, 2010; Chinsamy-Turan, 2012a; Padian & Lamm, 2013 for summaries). Until recent years and apart from a few seminal papers (Gross, 1934; Enlow & Brown, 1958; Warren, 1963; Klevezal, 1996), mammalian bone histology received little attention by biologists and palaeontologists alike compared to dinosaurs and non-mammalian synapsids (e.g., Horner, Ricqles & Padian, 1999; Sander et al, 2004; Chinsamy-Turan, 2012a; see Padian, 2013 for a review on Chinsamy-Turan, 2012a)

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