Myology of the masticatory apparatus of herbivorous mammals and a novel classification for a better understanding of herbivore diversity

Abstract

Masticatory muscle features allow for an understanding of how dietary habits and masticatory functions have evolved across mammalian lineages. Herbivorous mammals were traditionally classified as pertaining to either ‘ungulate-grinding’ or ‘rodent-gnawing’ morphotypes, but those classes might not adequately encompass the diversity of past and present herbivores. We compiled data for 104 herbivorous (nine orders, including new data for 31 species) and ten non-herbivorous (five orders) extant species and for four extinct taxa, in order to construct a more comprehensive scheme of masticatory morphotypes. A myological phylomorphospace revealed 15 morphotypes, which were tested statistically and interpreted morphofunctionally. Extant herbivorous morphotypes diversified along two main pathways that did not reflect the traditional types. Additionally, some extinct herbivores adapted along alternative pathways to those of extant forms. Early mammaliaforms and mammals possessed muscle proportions almost identical to those of living carnivores. Several more plesiomorphic herbivorous morphotypes were recognized, with some of them retaining generalized myological proportions. The rodent disparity was remarkable and could not be encompassed by a single category or pathway. Features of some derived euungulates and diprotodonts resembled rodents, but only a few extinct euungulates and extant wombats converged closely with them. Criteria for selecting models for palaeobiological reconstructions are discussed.

Masticatory myology of the llama (Lama glama, Camelidae) and comparisons with other camelids and euungulates

“…The large M. temporalis of early diverging artiodactyls represents a retention of the ancestral ungulate condition. This trait is also recorded in diverse extinct euungulates and, in different degrees, in generalized mammalian forms (Druzinsky et al, 2011;Ercoli et al, 2023;Janis, 1983;Joeckel, 1990;Lesbre, 1903;Popowics & Herring, 2006;Radinsky, 1985;Turnbull, 1970;Van Linden et al, 2022), including some non-ungulate herbivores (e.g., elephants, sloths; Druzinsky et al, 2011;Ercoli et al, 2023;Maglio, 1972;Naples, 1985;Turnbull, 1970). In line with this, the muscle reconstruction of two extinct artiodactyl entelodonts (Paleogene-early Neogene non-pecoran artiodactyls) performed by Joeckel (1990) indicates a larger M. temporalis (45 to 46%) than those of living artiodactyls (Figure 5).…”

“…To construct the comparative quantitative sample, we compiled available quantitative myological data on extant ungulates, and reconstructed muscle proportions of two extinct euungulate entelodontids from the literature (Endo et al, 2002;Ercoli et al, 2023;Furuuchi et al, 2013;Joeckel, 1990;Schumacher, 1961;Turnbull, 1970). For the sake of comparisons, relative weights of each masticatory muscle were computed as its mass divided by the total adductor mass following Ercoli et al (2023). After the final cleaning of materials for entry into the collection, crania and mandibles of specimens 1 and 2 were weighted using a Mettler Toledo pb1502-s balance, and the mean value of the weight ratio between masticatory muscle TA B L E 1 Wet masticatory muscle masses and bone masses in grams (g) for each muscle weighed for each side of the three Lama glama specimens.…”

“…Table 1 and Figure 5 show the relative muscle masses distribution of Lama glama in comparison with other euungulates (Endo et al, 2002;Ercoli et al, 2023;Furuuchi et al, 2013;Joeckel, 1990;Schumacher, 1961;Turnbull, 1970). other euungulates present smaller values for the M. temporalis than those observed in suines and camelids, and it is particularly reduced in some bovids and equids (≈17%-10%).…”

“…In line with this, the muscle reconstruction of two extinct artiodactyl entelodonts (Paleogene-early Neogene non-pecoran artiodactyls) performed by Joeckel (1990) indicates a larger M. temporalis (45 to 46%) than those of living artiodactyls (Figure 5). Thus, among the pool of extant taxa that more closely represents the plesiomorphic artiodactyl morphotype regarding the adductor masticatory configurations (named "suinomorphs" by Ercoli et al, 2023), Camelini instead of all camelids stand out as the most extreme representatives regarding the relative size of the M. temporalis (Figure 5).…”

“…Pterygoidei muscles have been recognized as well-developed and relevant for horizontal and particularly transverse component of movements during chewing in euungulate and ungulate-like herbivorous mammals (Ercoli et al, 2023;Maynard Smith & Savage, 1959;Popowics & Herring, 2006;Turnbull, 1970;Warburton, 2009).…”