Metabolism inferences
The pioneering work of Vizcaino et al. (2006) was based on the analysis of five giant sloth species from the Pampean Region (Argentina and Uruguay) from only two families, four mylodontids (Glossotherium robustum, Lestodon armatus, Mylodon darwini, and Scelidotherium leptocephalum), and one megatheriid Megatherium americanum. Mylodontids presented lower OSA values, whereas M. americanum had high OSA values. Vizcaino et al. (2006) suggest that the lower values of the mylodontids could indicate a higher level of fermentation in the digestive system and a possible lower metabolic requirement, while Me. americanum could present similar metabolic requirement to Epitherian taxa of the same size.
Dantas and Santos (2022) used the same approach to study giant sloths from the Brazilian Intertropical Region, that included all four sloth families, Megalonychiidae (Ahytherium aureum, Australonyx aquae), Nothrotheriidae (Nothrotherium maquinense), Mylodontidae (Glossotherium phoenesis, Ocnotherium giganteum, Catonyx cuvieri, Valgipes bucklandi), and Megatheriidae (Eremotherium laurillardi). The mylodontid and megathere giant sloths from BIR have OSA values higher than those from the Pampean Region and all taxa, with the exception of N. maquinense and O. giganteum, which fell on the regression line of epitherians, suggesting higher levels of oral food processing and metabolic requirements.
Excluding D. nordenskioldi and Mx. jeffersonii, all the megalonychids studied (Xibalbaonyx oviceps, Megalocnus rodens, Parocnus serus, Acratocnus ye, A. aureum, and Au. aquae), mylodontids (Paramylodon harlani, Glossotherium tropicorum, and Glossotherium wegneri), and megatheriids (Megatherium tarijense and Eremotherium laurillardi) had high OSA values that fell above the Xenarthra regression line (Fig. 5), showing the same pattern observed for giant sloths from BIR.
If this pattern is correct, all megalonychids may have had higher metabolic requirements than other sloths, which allows a review of the interpretation proposed by McDonald et al. (2013) for Megistonyx oreobios. The unique exception was D. nordenskioldi and Mx. jeffersonii, which fell on the Xenarthra regression, probably because of larger body mass relative to its OSA capability, which could have a direct effect, causing a high energy cost, probably lowering its metabolism.
The OSA × body mass of Nothrotheriops shastensis suggests that members of the Nothotheriidae probably had low oral food processing and metabolic requirements, together with D. nordenskioldi, Megalonyx jeffersonii, Ocnotherium giganteum, and the mylodontid species from the Pampean Region (Fig. 4). This hypothesis for Nh. Shastensis is supported by the size of plant fragments in its dung which are large and not fully chewed, may be related to long transit time in the gut to absorb nutrients (Lindsey et al., 2020).
Dantas and Santos (2022) proposed that giant sloths from temperate regions would have adapted to a lower oral food processing capability, together with a higher fermentation need. However, data from the North American temperate zones allowed us to disregard this hypothesis (Table 1; Fig. 4). This could reflect the evolution of North American taxa from tropical forms (McDonald, 2006; McDonald et al., 2017; Varela et al., 2019), and feeding on new types of vegetation promotes different metabolic requirements from giant sloths from the temperate zones of South America.
In terms of time to adapt to North American vegetation, Megalonyx jeffersonii would have had the greatest amount of time, Paramylodon harlani and Eremotherium laurillardi arrived later in Blancan, and Nothrotheriops shastensis was the last to reach North America and had the least amount of time to adapt, and all of these taxa reached more temperate latitudes in North America. Because Nohochichak xibalbahkah and Xibalbaonyx oviceps were restricted to in tropical habitats in North America, they do not appear to have adapted to different vegetation types in their diet.
Diet inferences
The Relative Muzzle Width index and hypsodonty index provide a means to suggest the different feeding adaptations of extinct giant sloths within the environment in which they lived, allowing an interpretation of their diet and habitat. These indices may allow for the interpretation of niche partitioning when multiple sloths are associated in a fauna, as well as how they may have avoided competition with other megaherbivores in the fauna.
The Hypsodonty index values (Table 1) did not differ between the extinct giant sloth families (ANOVA, F = 28.96, p < 0.05), suggesting adaptation to a similar degree of tooth wear between all taxa. As all sloths lack enamel on their teeth and the teeth are composed of similar types of dentine (Kalthof, 2011), as well as hypselodont and ever-growing, the rate of growth to compensate for tooth wear during mastication may be essentially the same in all sloths; therefore, the height of the teeth, as indicated by depth of the mandible, may not be a critical factor.
Available RMW values for the extinct giant sloths (Bargo et al., 2006; Dantas and Santos, 2022; Table S1) confirm the families Megalonychidae (13 species), Nothrotheriidae (two species), Mylodontidae (12 species), and Megatheriidae (three species) present different RMW values (Table 1). The unique exception was between Nothrotheriidae and Megatheriidae, which had similar values (ANOVA, F = 36.12, p < 0.05).
The RMW and HI values for megalonychid taxa showed an adaptation to a mixed-feeder to a browser diet (RMW = 0.35–0.85; HI = 0.65–1.32; Fig. 5). This partially agrees with the interpretation of a browser diet for members of this family (McDonald et al., 2017), for example, the diet of Xibalbaonyx oviceps is proposed to be composed of leaves and fruits (Stinnesbeck et al., 2021).
Unfortunately, only a limited number of other techniques can provide inferences on the diet of extinct species. However, dental microwear analyses have indicated that Acratocnus (Ac. odontrigonus) could have a mixed-feeder “browser” diet, while Megalonyx (Mx. wheatleyi) was a grazer (Resar et al., 2013). In marked contrast, carbon isotopic analysis of bioapatite and collagen (δ13Cap = -13.3‰; piC3 = 100%; δ13Ccol = -19.9‰; piC3 = 85%; Bocherens et al., 2004; McDonald et al., 2019; Table 1) suggest that Mx. jeffersonii is a browser. The same interpretation was made for Ahytherium aureum (δ13Cap = -14.4‰; piC3 = 100%; Costa et al., in press).
Both nothrotheres, Nothrotheriops shastensis and Nothrotherium maquinense, had RMW values indicative of adaptation as browsers (RMW = 0.66–0.74; Fig. 5), the HI values suggesting an adaptation to a less abrasive diet for N. maquinense (HI = 0.77; Table 1), but a high abrasive diet for Nh. shastensis (HI = 1.09; Table 1), confirmed by direct evidence of the diet by the diversity of plants it consumed in preserved coprolites (Hansen, 1978; Thompson et al., 1980).
Carbon isotopic values for N. maquinense (δ13Cap = -12.4 ± 0.06; piC3 = 96%; Omena et al., 2021; Table 1) and Nh. shastensis (δ13Ccol = -19.5 ± 0.02‰; piC3 = 82%; Fuller et al., 2014; Table 1) confirm a browser diet for both. In Nh. shastensis, microwear analysis (Green et al., 2009), coprolite analysis based on macrobotanical composition (Hansen, 1978), and molecular data (Hofreiter et al., 2000) reinforce this interpretation. However, the available carbon isotopic values in bioapatite indicate an opposite diet rich in C4 plants (δ13C = 1.7 ± 0.04‰; piC4 = 100%; DeSantis et al., 2019; Table 1).
The Mylodontidae species presented the widest RMW in comparison with the other families (RMW = 0.28–0.58; Table 1; Fig. 5), indicative of a mixed-feeder diet, in agreement with the results presented by Naples (1989). The only exception was L. armatus, which was adapted to the grazer diet (RMW = 0.28; Table 1). The HI values reinforce this interpretation, suggesting an adaptation to less abrasive food items (HI = 0.48–0.91; Bargo et al. 2006b; Table 1).
Currently the only taxa in the family, for which carbon isotopic data acquired from collagen and bioapatite is available are Glossotherium robustum, Catonyx cuvieri (from Brazil), Valgipes bucklandi (Brazil), Paramylodon harlani (United States), and Lestodon armatus (Uruguay).The data for these taxa indicate a mixed-feeder “browser” diet for G. robustum and C. cuvieri, and a browser diet (piC3 > 80%) for P. harlani, V. bucklandi, and L. armatus (Table 1). As occurred in Mx. jeffersonii, the carbon isotopic data acquired through bioapatite for Paramylodon harlani indicates a diet that is opposite to that indicated by the collagen analysis data (Ruez, 2005; Perez-Crespo et al., 2014; DeSantis et al., 2019; Table 1).
Finally, the HI index suggests that all megatherines were adapted to abrasive food items (HI = 0.50–1.02; Table 1), the RMW index suggesting that Eremotherium laurillardi and Megatherium tarijense were adapted to a mixed-feeder “browser” diet (RMW = 0.63–0.69; Fig. 5), whereas Megatherium americanum was a strict browser (RMW = 0.84; Fig. 5). The limited carbon isotopic (bioapatite) data from the E. laurillardi in Mexico (δ13C = -7.7‰; piC3 = 62%; Perez-Crespo et al., 2015; Table 1) seems to confirm this dietary pattern, however, the data from Brazil (bioapatite and collagen) suggest a mixed-feeder “grazer” diet (piC4 = 54–56%; Dantas et al., 2020; Omena et al., 2021; Table 1), These differences may reflect greater dietary flexibility in E. laurillardi, which may explain its wide latitudinal distribution and a range greater than any other sloth.
Microwear analyses of E. laurillardi in Brazil also confirmed a mixed-feeder diet (Oliveira et al., 2020). The carbon isotopic values of bioapatite and collagen suggest that Me. americanum had a mixed-feeder “browser” diet (piC3 = 60–71%; Bocherens et al., 2017; Lopes et al., 2021; Table 1).
Dantas (2022) discussed how body mass strongly influenced the variation in carbon isotopic values in giant sloths from the Brazilian Intertropical Region (n = 4; R2 = 0.90), which represented changes in habitat use and consequently their diet. However, body mass did not seem to affect the RMW index in giant sloths (n = 23; R2 = 0.30; Fig. 6A).
When all available δ13Ccollagen data for giant sloths from the Americas were interpreted together, a moderate correlation between δ13Ccollagen and body mass was observed (n = 7; R2 = 0.48; Fig. 6B), similar to that observed by Dantas (2022). However, δ13Cbioapatite showed no correlation with body mass (n = 10; R2 = 0.04; Fig. 6C), with results opposite to those reported by Dantas (2022). This occurs because of the discordant carbon isotopic data acquired through bioapatite found for Mx. jeffersonii (δ13C = 1.7 ± 0.04‰; Table 1) and P. harlani (δ13C = 3.3 ± 4.2‰; Table 1), which differ strongly from the carbon isotopic data found in collagen. Without these values, the correlation coefficient increased to 0.62.
Niche differentiation
The niche differentiation of the Late Quaternary giant sloths has been studied and currently we have a view that mostly Megalonychidae and Nothrotheriidae could be mainly climbers, the Mylodontidae mainly diggers, while the Megatheriidae were fully terrestrial animals (Bargo et al., 2000; Vizcaino et al., 2006; Santos et al., 2023).
Our results suggest that within the Megalonychidae, Acratocnus ye could be a suspensory species, while Parocnus serus, Mesocnus rodens, Xibalbaonyx oviceps, and Diabolotherium nordenskioldi were climber species (Fig. 7), with Pa. serus probably also being a digger species (Table 1). The results for D. nordenskioldi were in accordance with the interpretation made by Pujos et al. (2007). Unfortunatelly Megistonyx oreobios and Nohochichak xibalbahkah do not have preserved ulnae, which prevents us from proposing their ecological niche based on this bone.
As in the case of Mx. jeffersonii the larger body mass of Nothrotheriops shastensis probably prevented it from being considered to be a climber species (as N. maquinense, Fig. 7; Santos et al., 2023), it also was not a digger species (Table 1). It is possible that immature juvenile individuals of Megalonyx could climb until they reached a critical size, but the paucity of juvenile skeletons at different growth stages, prevents a resolution of this question at this time.
Within the Mylodontidae Mylodon darwini was probably a digger species, while Paramylodon harlani and Glossotherium wegneri were specialized diggers, as the species O. giganteum, G. phoenesis, L. armatus, and C. cuvieri. The Megatheriidae E. laurillardi from USA, does not differ from the South American relatives, being a fully terrestrial species, as expected (Fig. 7; Table 1).
Final remarks
The giant sloths which lived in southern South America, probably had a higher level of fermentation/lower metabolic requirement, which was reflected in the late Pleistocene taxa found in the Pampean Region. As these taxa migrated to tropical regions, they probably evolved higher metabolic requirements, and these tropical taxa migrated to Central and North America, explaining the pattern observed in this study.
We have a paradox here, the more southern giant sloths in South America would have been at higher latitudes and in the more temperate zones, as for example the Pampas in Buenos Aires Province is (34 to 38 degrees south), which is roughly the same latitude as the southern third of the United States. So sloths in these two regions are living in climatically comparable regions which is what Webb argued for in his savanna taxa interchange papers. We point out that tropical adapted sloths in southern Mexico and Central America did not move into temperate habitats.
The relative muzzle width and hypsodonty indices suggest dietary adaptation of several late Pleistocene/early Holocene giant sloths in the Americas. Nothrotheriidae and Megatheridae taxa were adapted to a browser or mixed-feeder “browser” diet, Mylodontidae taxa to a variety of diet types, and Megalonychidae taxa to a mixed-feeder to a browser diet. The Occlusal Surface Area index together with the body mass allows a better understanding of the paleoecology and evolution of the giant sloths in the Americas.
These dietary adaptations did not necessarily reflect their food niche; the RMW diets for some Mylodontidae taxa were different from what RMW and HI suggested. Similarities between RMW, HI, and isotope/microwear analysis were observed for Megalonychidae, Nothrotheriidae, and Megateridae taxa.
Finally, two indices based on ulna measurements allowed us to differentiate the ecological niche of giant sloths. A probable pattern is that Megalonychidae and Nothrotheriidae could include mainly climber species, while Mylodontidae taxa are mainly diggers, and Megatheriidae, due to their higher body mass, a fully terrestrial species.