Labelling experiments in red deer provide a general model for early bone growth dynamics in ruminants

Abstract

Growth rates importantly determine developmental time and are, therefore, a key variable of a species' life history. A widely used method to reconstruct growth rates and to estimate age at death in extant and particularly in fossil vertebrates is the analysis of bone tissue apposition rates. Lines of arrested growth (LAGs) are of special interest here, as they indicate a halt in bone growth. However, although of great importance, the time intervals between, and particularly the reason of growth arrests remains unknown. Therefore, experiments are increasingly called for to calibrate growth rates with tissue types and life history events, and to provide reliable measurements of the time involved in the formation of LAGs. Based on in vivo bone labelling, we calibrated periods of bone tissue apposition, growth arrest, drift and resorption over the period from birth to post-weaning in a large mammal, the red deer. We found that bone growth rates tightly matched the daily weight gain curve, i.e. decreased with age, with two discrete periods of growth rate disruption that coincided with the life history events birth and weaning, that were visually recognisable in bone tissue as either partial LAGs or annuli. Our study identified for the first time in a large mammal a general pattern for juvenile bone growth rates, including periods of growth arrest. The tight correlation between daily weight gain and bone tissue apposition suggests that the red deer bone growth model is valid for ruminants in general where the daily weight gain curve is comparable.

The origin of placental mammal life histories

“…3) and with the transition recorded in its limb bones (Extended Data Fig. 6), identical to weaning transitions recently described on the basis of fluorescent labelling 43 . Together, these lines of evidence constrain weaning in P. bathmodon to between 31 and 75 days after birth, with the weight of evidence supporting cessation of suckling by 2 months after birth.…”

“…1j,k), although laminations in this tissue are not as well developed as in the lamellar bone of the adult individual. This transition likely corresponds to changes in growth rate associated with weaning, as in living ungulates a similar transition occurs in some individuals over this interval 43 (see Supplement). The position of this transition partway through the cortex provides evidence for weaning in this individual prior to death at 2.5 months of age, supporting the 1-2 month suckling period suggested by dental trace elements and tooth wear.…”

“…Enamel secretion, crown extension, and crown formation rates were estimated using the methods of Dirks et al 47 Dietary trace element concentrations were assessed using laser-ablation inductively coupled-plasma mass spectroscopy (LA-ICP-MS) at the University of Edinburgh and the University of St. Andrews Isotope Geochemistry (STAiG) lab. After pilot runs using an ATLEX-I-LR Analyte Excite 193 nm ArF excimer coupled to an Attom ICPMS, Nu Instrument at the University of Edinburgh, to assess the suitability of the material for analysis, a broad array of trace element concentrations ( 11 B, 23 Na, 25 Mg, 27 Al, 31 P, 43 Ca, 46 Ca, 55 Mn, 59 Co, 60 Ni, 63 Cu, 66 Zn, -4). Small regions of interest in the deciduous teeth (NMMNH P-27844) were also scanned at high resolution (38 µm spot size, 38 µm s -1 scanning speed; Figs.…”

Osteohistology and palaeobiology of giraffids from the Mio‐Pliocene Langebaanweg (South Africa)

“…Despite the abundance of extant ungulate species, limb bone histology has only been conducted in a few taxa and has been focused mainly on modern artiodactyls. Some studies have focused on the assessment of life history traits such as, growth patterns and size in deer and reindeer (Singh et al, 1974 ), comparative growth of young sheep (Cambra‐Moo et al, 2015 ) and pigs (Mori et al, 2005 ), as well as on deer (Amson et al, 2015 ; Calderón et al, 2021 ; Calderón et al, 2019 ; Kolb, Scheyer, Lister, et al, 2015 ; Kolb, Scheyer, Veitschegger, et al, 2015 ), and more recently on Giraffa camelopardalis Linnaeus, 1758 (Smith, 2020 ). For example, Kolb, Scheyer, Lister, et al ( 2015 ) examined body size and growth in deer, whereas Skedros et al ( 1997 ) undertook several studies to examine the biomechanical properties of the metacarpals of equids (Skedros et al, 2003 ), calcanei of horses, elks and sheep (Skedros et al, 1997 ), as well as studies of the humerus, radius, metacarpal and phalanx of the rocky mountain mule deer (Skedros et al, 2003 ).…”