Paleobiology of Pleistocene ground sloths (Xenarthra, Tardigrada): biomechanics, morphogeometry and ecomorphology applied to the masticatory apparatus
M. Susana Bargo1 and Sergio F. Vizcaíno1
1CIC-CONICET. División Paleontología Vertebrados, Museo de La Plata, Paseo del Bosque s/n, 1900 La Plata, Argentina. msbargo@fcnym.unlp.edu.ar , vizcaino@fcnym.unlp.edu.ar
Abstract. The fossil xenarthrans include giant forms, the ground sloths (Tardigrada), characteristic of the mammal fauna of the Pleistocene of South America. Although most authors agree in considering them as herbivorous, these forms have not been studied in terms of detailed morpho-functional analyses of their masticatory apparatuses. The aim of this work is the study the masticatory apparatus of the large Pleistocene ground sloths Glossotherium robustum, Lestodon armatus, Mylodon darwini and Scelidotherium leptocephalum (Mylodontidae) applying biomecanichal and morphogeometrical methods, and to compare with the information obtained for Megatherium americanum (Megatheriidae). The results are integrated with recent ecomorphological analyses that include three variables (hypsodonty index, dental occlusal surface area and relative width and shape of the muzzle) providing useful information for the inference of dietary habits and to propose a niche partitioning among these species. Glossotherium robustum and Lestodon armatus, the wide-muzzled sloths, were mostly bulk-feeders (i.e. ingest great amounts of food with each bite; probably grass and herbaceous plants). Mylodon darwini and Scelidotherium leptocephalum, the narrow-muzzled sloths, were mixed or selective-feeders (i.e. select plants or plant parts; grass and/or tree and shrubs foliage). The tooth design of mylodontids indicates that teeth were used mainly for crushing and grinding turgid and fibrous items respectively. Megatherium americanum was probably the most selective feeder among these sloths, and selectively fed on particular plants (shrubs) or plant parts (leaves, twigs, fruits). Its dentition was designed mostly for cutting soft but tough items which might include flesh, leaving open the possibility of an omnivorous diet.
Resumen. Paleobiología De Los Perezosos Terrestres (Xenarthra, Tardigrada) Pleistocenos: Biomecánica, Morfogeometría Y Ecomorfología Aplicadas Al Aparato Masticatorio. Los xenartros fósiles incluyen formas gigantes, los perezosos terrestres (Tardigrada), características de la fauna de mamíferos del Pleistoceno de América del Sur. Si bien la mayoría de los autores los han considerado herbívoros, estas formas no han sido objeto de un análisis morfofuncional detallado de sus aparatos masticatorios. El objetivo de este trabajo es estudiar el aparato masticatorio de los perezosos terrestres Glossotherium robustum, Lestodon armatus, Mylodon darwini y Scelidotherium leptocephalum (Mylodontidae) aplicando métodos biomecánicos y morfogeométricos, y compararlos con Megatherium americanum (Megatheriidae). Estos resultados son integrados con aquellos obtenidos de análisis ecomorfológicos que incluyen tres variables (índice de hipsodoncia, área de la superficie oclusal dentaria y ancho relativo y forma del hocico), proveyendo información para inferir probables hábitos alimenticios y proponer una partición de nichos. Glossotherium robustum y Lestodon armatus, formas de hocico ancho, no eran selectivos, se alimentaban al bulto (i.e. ingerían grandes cantidades de alimento con cada bocado; probablemente pastos y plantas herbáceas). Mylodon darwini y Scelidotherium leptocephalum, formas de hocico angosto, eran selectivos o intermedios (i.e. seleccionaban plantas o partes de plantas; pastos y/o hojas de árboles y arbustos). El diseño de los dientes indica que eran usados principalmente para triturar y moler alimentos semiduros o pulposos y fibrosos. Megatherium americanum era el más selectivo, y probablemente se alimentaba seleccionando ciertas plantas o partes de plantas (hojas, ramas, frutos). Sus dientes estaban diseñados principalmente para cortar alimentos blandos pero resistentes, que podrían incluir carne, lo que deja abierta la posibilidad de una dieta omnívora.
Key words. Mammalia; Xenarthra; Tardigrada; Paleobiology; Masticatory apparatus.
Palabras clave. Mammalia; Xenarthra; Tardigrada; Paleobiología; Aparato masticatorio.
Introduction
Sloths (Xenarthra: Tardigrada) are among the most conspicuous mammals in the Cenozoic faunas of South America and, as a group, they show a great diversity (with more than 80 genera, grouped in four families: Megatheriidae, Megalonychidae, Nothrotheriidae and Mylodontidae). During the early Miocene, the frequency and diversity of tardigrades increased considerably, including small to medium sized facultative arboreal forms (Scillato-Yané, 1986; White, 1997; McDonald and De Iuliis, 2008). But it is not until the Pleistocene, that a great number of gigantic sloths (Mylodontidae and Megatheriidae) are recorded. Webb (1985) proposed the term ground sloth for these forms belonging to different clades that reached the late Pleistocene-early Holocene. At present, tardigrades are represented only by two convergent genera: Choloepus (Illiger, 1811), the twotoed sloth, allied with members of Megalonychidae, and Bradypus (Linnaeus, 1758), the three-toed sloth, and the sister taxon of all the remaining sloths (Gaudin, 2004; figure 1). Carlini and Scillato-Yané (2004: 434) proposed a different view, considering that Bradypus differentiated through a process of heterochrony within Megalonychidae.
Figure 1. Phylogeny of Tardigrada (modified from Gaudin, 2004)
/ filogenia de los Tardigrada (modificado de Gaudin, 2004).
Although most authors agree in considering
ground sloths as herbivorous, the South American
forms have not been studied in terms of detailed
morpho-functional analyses of their masticatory apparatuses.
For more than a century general speculations
on the dietary preferences of ground sloths
have been proposed. Owen (1842, 1860) made remarkable
descriptions of the skeletons of the ground
sloths Glossotherium Owen, 1839 and Megatherium
Cuvier, 1796, and gave extensive explanations about
their possible diet and behavior. He based his conclusions
on the morphology of the skull, combined
with peculiarities of the rest of the skeleton, but always
by analogy with living tree sloths primarily,
and with other herbivorous extant mammals of similar
size (i.e. elephant, giraffe). Owen (1842:159-160)
wrote: …"The close correspondence between the
Megatherium and the Mylodon [Glossotherium] in the
modifications of the skeleton determining the peculiar
forces acting from the hind upon the fore-parts,
compels us to infer that they resembled each other in
the mode of which they obtained their sustenance;
and nevertheless, the difference in the form of the
grinding surface of the teeth, as well as in their size
and the depth of insertion, obviously indicates some
difference in the substances comminuted… On the
theory that the Megatherioids subsisted on foliage, it
is most natural to suppose that the Mylodon and
Megalonyx, with teeth most closely resembling those
of the Sloths, would feed, like them, on the leaves
and tender buds; while the Megatherium, whose essentially
bradypodal teeth were more modified by
their arrangement in a closer series, …so as concurrently
to offer and obvious resemblance to the
Elephant's dentition, would be thereby able to bruise
the smaller branches, and to masticate these together
with the buds and leaves"… "All the characteristics
which co-exist in the skeleton of the Mylodon and the
Megatherium conduce and concur to the production
of the forces requisite of uprooting and prostrating
trees;…" Latter in 1860, Owen stated about
Megatherium …"Guided by the general rule that animals
having the same kind of dentition have the
same kind of food, I conclude that the Megatherium
must have subsisted, like the Sloths, on the foliage of
trees; but that the greater size and strength of the
jaws and teeth, and the double-ridged grinding surface
of the molars in the Megatherium, adapted it to
bruise the smaller branches as well as the leaves, and
thus to approximate its food to that of the Elephants
and Mastodons".
Stock (1925) proposed that megatheres, together
with megalonychids and nothrotheres, were probably
browsers, while mylodontids were grazers. Cabrera
(1926) discussed the diet of Megatherium, rejecting
some theories on myrmecophagy or insectivory,
and entirely concurred with Owen's statements on a
folivorous diet. Winge (1941: 364) pointed that
Megatherium "has progressed farthest in specialisation
as a plant feeder" and that it "must undoubtedly
have fed on unusually tough leaves which required
much power of mastication". Scillato-Yané (1977) indicated
that the Megatheriinae and Mylodontidae
had a robust calcaneum, which might be used as a
steady point to dig with the fore limbs to root out the
grasses, which were the basis of their diet.
More recently, dietary habits were proposed based
on some features of the masticatory apparatus.
McDonald (1987) indicated that the Plio-Pleistocene
South American Scelidotheriinae were selective-feeders
because the long and narrow muzzle was appropriate
to select plant parts. For the North American
ground sloths, Naples (1987, 1989) proposed
that Nothrotheriops shastense (Sinclair, 1905) (Nothrotheriidae)
was a selective browser and Paramylodon
harlani (Owen, 1843) (Mylodontidae) a browser/
grazer, instead of a strict grazer. McDonald (1995)
considered that Megalonyx Harlan, 1825 (Megalo-
nychidae), also from North America and Eremotherium
Spillmann, 1948 (Megatheriidae), from North
and South America, were browsers.
An alternative hypothesis to the ground sloths
herbivory was proposed by Fari ña (1996) on the basis
of a study that analyses the trophic relations of the
Lujanian (late Pleistocene, early Holocene) megafauna.
Fariña suggests that the ground sloths might
have been opportunistic scavengers, especially Megatherium
americanum (Cuvier, 1796). Fariña and Blanco
(1996) support this hypothesis indicating that
Megatherium was probably an active hunter based on
the development of the olecranon process, which
would allow it to stab effectively the prey.
In the last decade, several studies on the paleobiology
of South American mammals, mostly xenarthrans,
were conducted based on morpho-functional
and biomechanical analysis of the feeding apparatus
(Fari ña, 1985, 1988; Vizcaíno, 1994; Vizcaíno
and Fariña, 1997; Vizcaíno and Bargo, 1998; Vizcaíno
et al., 1998; De Iuliis et al., 2000; Pérez et al., 2000;
Bargo, 2001a and b; Fariña and Vizcaíno, 2001;
Vizcaíno and De Iuliis, 2003; Bargo, De Iuliis and
Vizcaíno, 2006; Bargo, Toledo and Vizcaíno, 2006;
Vizcaíno, Bargo and Cassini, 2006), and their paleoecological
context, specially referred to the trophic relations
(Fariña, 1996; Vizcaíno, 2000; Vizcaíno et al.,
2006).
The great variation in skull and dental morphology,
body size and proportion among ground sloths
suggests that they had diversified to fill a variety of
niches. Their marked differences in the skeletal and
dental anatomy with other mammalian herbivores,
and the lack of recent analogs, makes difficult to interpret
the ecology of ground sloths, particularly
their dietary habits. Even the extant tree sloths are
too specialized to provide good models: with relative
small body masses (less than 10 kilograms), they are
strictly arboreal, folivorous (consuming mainly tree
and liana leaves), and extremely silent during their
rare and careful movements, spending most of their
time well-hidden in the high canopy of Neotropical
forests (Chiarello, 2008).
Several studies on the biomechanics of the masticatory
apparatus have demonstrated correlations
among the behavior, diet, and form of the skull, jaws,
dentition, and musculature in extant mammals ( e.g.,
Maynard Smith and Savage, 1959; Turnbull, 1970;
Moore, 1981; Naples, 1982, 1985; Smith, 1993;
Spencer, 1995; Mendoza et al., 2002; Mendoza and
Palmqvist, 2007, 2008). Particularly, Janis (1995) proposed
that there are three variables that allow discriminating
among ungulates of grazing, browsing
and mixed feeder habits: hypsodonty index, lower
premolar row relative length, and the relation between
palatal width and muzzle width. However, it
is worth mentioning that recently Mendoza and
Palmqvist (2007, 2008) detected at some exceptions -
e.g. the white rhino, Ceratotherium simum (Burchell,
1817)- to these generalizations considering each variable
individually (see Discussion). In several recent
papers we analyzed and adapted these variables (see
Discussion) to the morphology of the tardigrades in
order to facilitate their application to these mammals.
(Bargo, De Iuliis and Vizcaíno, 2006; Bargo, Toledo
and Vizcaíno, 2006; Vizcaíno, Bargo and Cassini,
2006).
This work summarizes the Doctoral Thesis of one
the authors (Bargo, 2001a) as a review of the already
published subjects, with the addition of the unpublished,
updated, and improved information and results.
The goal is the study of the morphology of the
masticatory apparatus of the large Pleistocene mylodont
ground sloths Glossotherium robustum (Owen,
1842), Lestodon armatus Gervais, 1855, Mylodon darwini
Owen, 1839 and Scelidotherium leptocephalum
Owen, 1840 (Mylodontidae) applying biomecanichal
and morphogeometrical methods, and compare
these taxa with Megatherium americanum (Megatheriidae;
Bargo, 2001b) (figure 2). The results obtained
are then integrated with recent ecomorphological
analyses of these ground sloths, including the hypsodonty
index (Bargo, De Iuliis and Vizcaíno, 2006),
the dental occlusal surface area (Vizcaíno, Bargo and
Cassini, 2006) and the relative width and shape of the
muzzle (Bargo, Toledo and Vizcaíno, 2006), providing
useful information for the inference of different
dietary habits and, hence, allowing us to propose a
paleoecological interpretation (niche partitioning) of
the Pleistocene tardigrades.
Figure 2. 1, Glossotherium robustum (MLP 3-140). 2.2, Lestodon armatus (MLP 3-30). Scale bar / escala: 10 cm. 3, Mylodon darwini (CN
43).4, Scelidotherium leptocephalum (MLP 3-402). Scale bar / escala: 5 cm. 5, Megatherium americanum (MNHN PAM 276). Scale bar / escala: 10 cm.
The use of terms browser and grazer
As becomes evident from the previous section,
most authors refer to the dietary habits of fossil
sloths as grazers or browsers. In some cases, they also
use the feeding category of mixed-feeders.
However, as noted in studies on living herbivores
(Hofmann and Stewart, 1972; Spencer, 1995), the
terms browsing and grazing are of ambiguous nature.
A review of the literature available on the subject
reflects that the terms have been used to refer to
the mode of food acquisition, as well as the type of
food ingested, i.e. "browsing" may refer to selective
feeding of any food type, as well as eating dicot material;
"grazing" denotes grass eating, but is used to
mean eating of forbs as well. Nature provides plenty
of examples of these "ambiguities". For instance, the
living cervid Ozotoceros bezoarticus (Linnaeus, 1758)
which feeds mainly on grasses, but also plucks small
morsels from nutritious plants of certain species,
would be a browser from the point of view of the
food acquisition and a grazer considering only the
food ingested. Consequently, when applied to an extinct
species -and to great extent also to living animals-,
the reader (and probably the authors themselves)
do not know if the terms refer to a mode of
food acquisition selected by size and shape, and so is
independent of the taxonomic nature of the item
within certain ranges (i.e. herbivory), or the selection
of specific taxa independent of the size and shape, or
an uncertain degree of combination of both.
It seems that the basic problem while trying to
classify mammals as either browsers or grazers is
that both terms are based in different criteria, as it becomes
apparent considering the meaning of the
words. On one side, browse reflects capacity for
searching and is used for feeding on leaves, young
shoots, and other vegetation independently of its taxonomy
(although it's definition also includes grazing
among its meanings). On the other, graze implies
some taxonomic, as well as structural constraints: to
feed on growing grasses and herbage.
Hofmann and Stewart (1972) proposed a classification
for ruminant ungulates as bulk and roughage
eaters (grass eaters, and within them roughage grazers;
fresh grass grazers; and dry regions grazers), selectors
of concentrate juicy herbage (with tree and shrub
foliage eaters, and fruit and dicot foliage selectors),
and intermediate feeders (with some preferring grasses,
and other preferring forbs, and shrub and tree foliage).
This alternative classification was based on the
stomach-structure and feeding habits of East African
ruminants, but in some way it reflects physical properties
of the consumed plants. It was proposed that
bulk-feeders eat low quality plant material, and that
this correlates with wide-muzzled animals to improve
the quantity of food intake in each bite, while
selective-feeders are narrow-muzzled facilitating selection
of more nutritious small plant or plant parts
(Janis and Ehrhardt, 1988; Solounias et al., 1988;
Solounias and Moelleken, 1993). From this point of
view, the previously mentioned cervid Ozotoceros bezoarticus
would be a selective feeder, and its morphology
clearly correlates with that behavior
(Merino et al., 2005).
Following Solounias and Moelleken (1993), the
terms grazers and browsers should be used specifically
to express types of vegetation eaten, not to distinguish
between selective and non-selective feeders.
However, to assign a type of vegetation eaten is difficult
if behavior is not observable and isotopic
analyses are not available. In some cases, as the complex
multivariate approach by Mendoza et al. (2002),
observations on eaten food are highly statistically
correlated to craniodental features for living ungulates.
But, as the same authors pointed out, the discrimination
of feeding habits in ungulates is a rather
difficult task, due to functional, historical and biomechanical
constraints, features that are highly emphasized
in forms so distant phylogenetically, with almost
no living relatives or evident analogs.
In an attempt to escape to this dead end, we analyze
morphology based on a mechanical assessment
(e.g. relationships between strength and speed, etc)
and hence on how it deals with physical properties
(hardness, wearing, size). Plotnick and Baumiller
(2000) stated that this paleobiomechanic approach
does not indicate if an organism has an optimal design,
but determines whether structures were capable
of doing a given function. Following this criterion,
we will refer to dietary habits of ground sloths on
the basis of the main physical properties of the food
inferred from the morphological evidence.
Materials and methods
For the purpose of this study, nearly thirty skulls
(most of them very complete) from different institutions
from Argentina and abroad were examined.
The acronyms and material studied are listed in
Appendix 1.
The skull morphology of the mylodontids G. robustum,
L. armatus, M. darwini and S. leptocephalum
was described and then compared through morphogeometric
methods. The masticatory muscles were
reconstructed for the jaw mechanics analysis, and the
occlusal patterns and mandibular movements determined
through study of the craniomandibular joint,
the form and arrangement of the dentition, including
occlusal wear patterns, and the form and structure of
the mandibular symphysis. These results were compared
with those obtained by Bargo (2001b) for M.
americanum.
Skull morphology and shape analysis. The morphology
of the skull, mandible and dentition of the
ground sloths were described comparatively, emphasizing
only on those features that are relevant for
the biomechanical analysis. The shapes of the skull
and mandible were then compared using a morphogeometric
method, which allows determining patterns
of morphological variability and change. A superimposition
technique (RFTRA, Resistant-Fit Theta-
Rho-Analysis) was used. It analyzes changes in
shape through the superimposition of one form onto
another (base and target specimen, respectively) using
the position of landmarks (homologous and geometrical
points, or type I and II landmarks respectively
sensu Bookstein, 1981) (see Benson et al., 1982;
Chapman, 1990a and references therein). The distance
coefficients obtained allow constructing distance
matrices that, through a cluster analysis using
UPGMA (Unweighted Pair-Group Method with
Arithmetic Averages) generate dendrograms. RFTRA
identifies and measures the homologous regions
of change in shape by establishing congruence
among those that have not changed. Although RFTRA
has been applied especially to identify shape
variability in a taxonomical context (Chapman,
1990b), recent studies on xenarthrans demonstrated
this approach as useful in morpho-functional interpretations
(Vizcaíno and Bargo, 1998; Vizcaíno et al.,
1998; De Iuliis et al., 2000; Vizcaíno and De Iuliis,
2003).
Comparisons of pairs of specimens (skulls in lateral
and palatal views, and mandibles in lateral
views) of the four mylodontids were performed. In
all cases, Glossotherium robustum was used as the base
specimen. For this purpose, 19 landmarks (12 homologous,
and 7 geometric were chosen for the lateral
and palatal views of the skull, and 14 landmarks (5
homologous, and 9 geometric) for the lateral view of
the mandible (Appendix 2, figure 3). Comparisons of
G. robustum - M. americanum were performed and illustrated
by Bargo (2001b: 186, figure 7).
Figure 3. Skull in lateral (1) and palatal (2) views, and mandible
in lateral view (3) of Glossotherium robustm showing the landmarks used for the morphogeometrical (RFTRA) analysis / cráneo en vista lateral (1) y palatal (2) y mandíbula en vista lateral (3) de Glossotherium robustum mostrando los landmarks utilizados para el análisis morfogeométrico (RFTRA).
Masticatory musculature. Muscle attachment sites are usually unambiguously indicated in mammals by
features of the skull and jaws, such as roughened surfaces,
scar lines, ridges, and crests. These features are
usually more conspicuous in fossil than in living
mammals, but the identification of them depends on
the size of the fossil specimen, on their degree of
preservation and the ontogenetic age of the individual.
The areas of origin and insertion of the masticatory
muscles were reconstructed based on these features,
and the patterns of musculature in modern
mammals (Maynard Smith and Savage, 1959;
Turnbull, 1970), particularly those in tree sloths
Bradypus and Choloepus (Macalister, 1869; Windle
and Parson, 1899; Edgeworth, 1935; Sicher, 1944;
Naples, 1982, 1985). Naples (1987, 1989) reconstructed
in great detail the masticatory muscles, including
the subdivisions of the m. temporalis, m. massetericus
and m. pterygoideus of Nothrotheriops shastense and Paramylodon
harlani. The material described by Naples,
which one of the authors (MSB) was able to study,
comes from the collection made from the Rancho La
Brea Tar Pits housed at the Page Museum. The skulls
and mandibles of these ground sloths are extremely
complete, with an excellent degree of preservation,
but the skulls and jaws recovered from the tar pits
were disarticulated, and in most cases, it is not possible
to establish individual correspondences between
skulls and jaws from the same individual.
The nature and relationships of the skeletal features
in the material examined for this work preclude
as confident a reconstruction of the musculature detail
that Naples was able to achieve. In any event, the
scope of this paper does not require such detail reconstruction.
Thus, only those features of the musculature
that are relevant for analysis of the lines of action
are described here. The musculature reconstructed
for this analyses includes the m. temporalis,
m. massetericus (including the m. zygomaticomandibularis),
and m. pterygoideus.
Jaw mechanics. The application of biomechanics to
the study of fossil vertebrates has proven to be a
good approach to the testing of functional hypothesis
(Plotnick and Baumiller, 2000). In this way, the jaws
can be considered as a lever system, with the pivot at
the craneomandibular joint, and the masticatory
muscles providing the input force, whereas the output
force is produced by the teeth on food. Then, the
moment arms of the lines of action of the masticatory
muscles can be estimated to analyze relationships
between bite force and velocity. This procedure was
applied to recent mammals (Maynard Smith and
Savage, 1959; Turnbull, 1970), and then to fossils with
a new geometric model proposed by Vizcaíno et al.
(1998), which allows comparisons between fossil and
extant mammals (figure 4). De Iuliis et al. (2000) and
Vizcaíno and De Iuliis (2003) used this methodology
with fossil giant armadillos, and Bargo (2001b) with
the ground sloth Megatherium americanum. Total
lengths of the mandibles were standardized at 11 cm
to allow comparison among specimens of different
sizes. Once the areas of origin and insertion of the
masticatory muscles are reconstructed, the moment
arms of the lines of action of the m. temporalis and m.
massetericus can be estimated, based on the calculation
of the averages of a given number of moment
arms, generated from different points in the origin
and insertion areas of each muscle. Due to the dorsoventrally
expanded shape of the jugal in sloths, the
different points of the origin of the m. massetericus
were located in the upper, middle and lowest point
(figure 4), which correspond to the posterior, middle
and anterior points in armadillos. In this way, the
values of the moment arms can be obtained independently
of the localization of the line of action, which
is difficult to determine in fossils. Interpretations on
the relationships between bite force and velocity may
be made by comparing the proportions of the combined
moment arms of the m. massetericus and m. temporalis
to those of different tooth positions (i.e., the
anteriormost, middle, and posteriormost teeth).
The analysis of teeth wear facets complements the
mechanical analysis since it can be used to infer the
direction of the mandibular movement during mastication
(Greaves, 1973; Rensberger, 1973; Costa and
Greaves, 1981). In extant mammals, the main jaw
movement during the power stroke is upward and
anteromedially directed (Hiiemae, 1978). Secondarily,
an increase of distinct components occurs in different
groups (e.g. anterior in rodents, vertical in carnivores,
and lateral in herbivores). During these movements,
teeth wear facets are produced, indicating
the main direction of the jaw movement. Two types
of wear facets can be described: those produced by
tooth-tooth contact -which might have striations, indicating
the orientation but not the direction of the
movement- and those produced by tooth-food-tooth
contact, characterized by the absence of striations.
Also, the leading and trailing edges and leading and
trailing interfaces can be identified. The interfaces
enamel-dentine, continuous and discontinuous, indicates
more clearly the direction of the upper and lower
molar to each other during the masticatory movement.
Figure 4. 1, Geometric model used for the estimation of moment
arms of the masticatory muscles in Glossotherium robustum. Moment arms of the m. massetericus (Mm 1 to 5) from the middle
point of the origin area of the muscle on the zygomatic arch / Modelo geométrico utilizado para estimar los brazos de momento de los músculos masticatorios en Glossotherium robustum; Brazos de momento del m. massetericus (Mm 1 a 5) a partir del punto medio del área de origen del m. massetericus sobre el arco cigomático; 2, from the anterior
most point of the origin area / a partir del punto más anterior del área de origen; 3, and from the posterior most point of the origin
area / y a partir del punto más posterior del área de origen; 4, Moment
arms of the m. temporalis (Mt 1 to 3), and the bite (Mb 1 to 3, from
the posterior most, middle and anterior most tooth respectively) / Brazos de momento del m. temporalis (Mt 1 a 3) y de la mordida (Mb 1 a 3 desde el diente más posterior, medio y más anterior, respectivamente.
Lines of action of the muscles / Líneas de acción de los músculos Moment arms of the m. massetericus and m. temporalis / Brazos de momento del m. massetericus y m. temporalis. Moment arms of the bite / Brazos de momento de la mordida).
Ferigolo (1985) analyzed the internal structure of the xenarthrans teeth. Sloth's teeth lack enamel, and are composed of three tissues: an external layer of cementum, a thin layer of hard dentine, and a modified soft dentine, which has low resistance to abrasion, forming the core. The cementum and soft dentine are easily abraded, leaving the hard dentine, interposed between these two tissues. Wear facets with the leading and trailing edges, and especially the continuous and discontinuous interfaces, can be observed between both types of dentine. This methodology was applied by Naples (1982, 1989) in living tree sloths and Paramylodon harlani, respectively. In this study, wear facets and striations were analyzed in numerous lower teeth series of Glossotherium robustum, in order to contrast with the observations in Paramylodon by Naples (1989) and then compared with the other mylodontids and M. americanum.
Results
Cranial morphology
Extensive descriptions of the skulls of ground
sloths were given by Owen (1842, 1856, 1857), Lydekker
(1886, 1894), Ameghino (1889) and Kraglievich
(1922, 1923, 1928 y 1934). McDonald (1987), De Iuliis
(1996) and Esteban (1996) included detailed anatomical
descriptions in their systematic revisions of the
Scelidotheriinae, Megatheriinae and Mylodontinae,
respectively. Naples (1989) studied the masticatory
apparatus of Paramylodon harlani, describing in detail
the skull and masticatory muscles in order to infer
feeding behavior and diet.
The skulls of ground sloths show a number of osteological
features that vary among different groups
of tardigrades, but taken as a whole, distinguish
them clearly from the rest of mammals: edentulous
premaxillae, loosely fused to the maxillae (with the
exception of Scelidotherium and Megatherium, were is
generally strongly attached to the skull); elongated
maxillae; incomplete postorbital bar, open zygomatic
arch, with ascending and descending processes of
the jugal well developed; pterygoids expanded as
thin blades; mandible with a long predental space,
with the length variable within the different groups.
The dental morphology of sloths is also extremely
different from other placental mammals, making difficult
to establish tooth homologies. The most characteristic
features are the lack of enamel, as well as the
lack of deciduous dentition and the cuspation pattern
observed in other mammals. Teeth are homodont
(so called molariforms or caniniforms), hypsodont
and ever growing (i.e., hypselodont), strongly
reduced in number (dental formula is 5/4, except in
Mylodon with 4/4 and the Pleistocene nothrotheres
with 4/3) and separated by diastema variable in
length.
This section presents comparative descriptions of
the four species of mylodontid considered in this
study, but only of those features of the cranium that
are relevant for analysis of the mechanics of the masticatory
apparatus. For a description of the skull of
Megatherium americanum see Bargo (2001b).
Skull. The skull shape of Glossotherium robustum and
Lestodon armatus is prismatic-rectangular and anteriorly
widened, with L. armatus the larger of the two
taxa (figures 2.1, 2). In both species the rostrum
(muzzle) is formed mostly by the maxillae, quadrangular
in lateral view, which bear anterior flanges,
very convex and upwards and posteriorly directed,
for the insertion of the caniniforms. In L. armatus the
caniniforms are larger than in G. robustum, and anteriorly
or mesially located from the first molariform,
resulting in a longer diastema (figures 5.1, 3). The
premaxillae of G. robustum and L. armatus are small,
arrow-head shaped, with the posterior medial
processes that attach loosely to the premaxillary
processes of the maxillae. This feature contributes to
the frequent loss of these bones in the specimens. The
skull of Mylodon darwini is large, like L. armatus, rectangular
shaped but much more elongated. The increase
in length is reflected in the anterior portion
(muzzle), due to an elongation of the premaxillae,
maxillae and nasals, as demonstrated by the morphogeometric
analysis (see below). M. darwini is
clearly distinguishable from the other mylodontids
because of the presence of a robust nasal arch in ontogenetically
older individuals: the premaxillae,
more robust than those of G. robustum and L. armatus, is firmly fused to the maxillae and extended dorsally
to reach the nasals, forming an unusual complete
arch, extensively described by Kraglievich (1934)
(figures 2.3 and 6.1). The region of the muzzle is more
elevated in comparison with the posterior part of the
skull, a feature clearly observed in lateral view.
Scelidotherium leptocephalum has a smaller skull, elongated
and very narrow in comparison with the above
mentioned mylodontinae (figures 2.4 and 6.3). The
rostrum is longer than the posterior part of the skull,
due to an elongation of the maxillae and specially the
premaxillae, a feature clearly observed in the shape
analysis performed. The premaxillae are also Vshaped,
but unlike the mylodontines, the lateral rami
are longer and deep. As in M. darwini, the premaxillae
are strongly fused to the maxillae, so they are preserved
with the skull in almost all specimens. An ascending
process is observed in some specimens in
the dorsal and medial part of the premaxillae, apparently
supporting the nasal cartilage (Bargo et al.,
2006). McDonald (1987) reported one specimen with
the nasal cartilage ossified, forming a structure analogous
to that of M. darwini.
Figure 5. Glossotherium robustum skull (1) and mandible (2) in
occlusal view. Lestodon armatus skull (3) and mandible (4) in occlusal
view / Glossotherium robustum cráneo (1) y mandíbula (2) en vista oclusal. Lestodon armatus cráneo (3) y mandíbula (4) en vista oclusal. Scale bar / escala: 10 cm.
Figure 6. Mylodon darwini skull (1) and mandible (BM(NH) M-
16617 Holotype) (2) in occlusal view. Scelidotherium leptocephalum skull (3) and mandible (4) in occlusal view / Mylodon darwini cráneo (1) y mandíbula (BM(NH) M-16617 Holotipo) (2) en vista oclusal. Scelidotherium leptocephalum cráneo (3) y mandíbula (4) en vista oclusal. Scale bar / escala: 10 cm.
The zygomatic arch is very conspicuous in all
ground sloths, and very similar in form in all of the
mylodontids considered here (figure 2). Unfortunately,
it is a frequently missing piece in fossils due to
the fragility of the joint between the zygomatic
process of the maxilla and the jugal. The jugal is expanded
posteriorly in a vertical plate, with three or
four processes. The ascending and descending
processes are well developed, and their orientations
vary slightly. The ascending process curves posteriorly,
while the more expanded descending process is
ventral and posteriorly oriented, showing in some
species (e.g. S. leptocephalum) two or three small
processes. The intermediate process is usually short,
with a pointed apex directed slightly ventrally. The
zygomatic process of the squamosal is a digitiform
structure. The anterior and posterior parts of the arch
are very close in all mylodontids, but never fuse so
that the arch is incomplete, unlike Paramylodon or
Megatherium, in which a secondary connection is
formed.
The pterygoids do not differ markedly in the four
considered species. They are inflated in their posterior
part, and form expanded bones ventrally, like thin
blades, with the ventral border rounded. The external
surface is roughened, with many scars for the origin
of the m. pterygoideus.
The palate is sub triangular in G. robustum and L.
armatus (with the anterior the widest part ), less triangular
in M. darwini, and parallel and very narrow
in S. leptocephalum (figures 5 and 6). In all species it is
flat in the transverse axis, but convex in the anteroposterior
axis. It is located almost at the plane of the
teeth occlusal surface, covering the lingual side of the
teeth by a well marked flange, although the crowns
of the teeth are visible on the labial surface of the
maxillary border. The palate shows a marked roughened
surface with many foramina (vascular perforations),
and a V-shape notch in the anterior edge for
the articulation of the premaxillae.
Craniomandibular joint (CMJ). The CMJ does not
vary in its general morphology in the taxa here examined.
It is located at the level of the occlusal plane,
or just slightly over it. The glenoid fossa is poorly defined,
with a shallow depression on the squamosal
process which allows the mandibular condyle great
freedom of motion (figures 5.1, 3 and 6. 1, 3). The
mandibular condyle is also positioned at the level of
the occlusal plane. It is wider mediolaterally than anteroposterioly,
projecting farther medially than laterally
relative to the coronoid process, and bears a
short neck (figures 5.2, 4 and 6.4).
Mandible. The form of the mandibles of G. robustum
and L. armatus do not differ markedly. The horizontal
ramus is very deep at the level of the last molariform,
decreasing gradually toward the caniniform,
and increasing slightly again until the anterior border
of the symphysis, which is situated at the occlusal
surface level. The ventral border of the horizontal
ramus is straight. The symphysis is strongly
fused, as in all sloths, and elongated (the predental
space is about half length of the dental series). It is elevated
from the horizontal, in an angle of about 45º,
but not surpassing the teeth occlusal plane. In occlusal
view, the symphysis is very wide (particularly
in L. armatus) with the anterior border slightly convex
or some times straight (figure 5). The mandibles
of M. darwini and S. leptocephalum are more elongated
and slender than those of G. robustum and L. armatus.
The elongation is produced in the predental
space, as demonstrated by the shape analysis (see below),
confirming a narrow and elongated predental
spout (longer than the dental series) (figure 6), elevated
over the teeth occlusal plane. The horizontal
rami are also deep at the level of the last molariform,
decreasing gradually to the anterior part.
The ascending rami are quite similar in the most
relevant features of the four species. The angular area
is prominent, expanded ventrally, surpassing slightly
the ventral border of the horizontal ramus. The lateral
surface is convex, showing well marked crests
for the insertion of the m. massetericus, while the medial
surface is concave. The angular process lies below
the level of the occlusal plane. The coronoid
process has a wide base, and it is not very high. It rises
very inclined above the condyle, and then curves
posteriorly.
Dentition. The dental formula is 5/4, except in Mylodon
darwini, which has 4/4, due to the lost of the first
upper molariform. Glossotherium robustum and
Lestodon armatus posses a canine-like first tooth,
termed the caniniform. The upper and lower dental
series converge backwards in G. robustum, L. armatus
and, in less degree, in M. darwini, while in S. leptocephalum
they are parallel.
As mentioned above, sloth's teeth are composed
of three types of tissues: cementum, and hard and
soft dentine. In mylodontids, the outer layer of cementum
is thin, and the occlusal surfaces of the molariforms
are concave, due to the central soft dentine
basin. The outer hard dentine forms sharp cutting
edges (figure 7.1). In contrast, Megatherium americanum
has an extremely thick layer of cementum
which, together with the soft dentine, is easily abraded,
leaving the hard dentine interposed between
these two tissues, forming sharp, transverse crests
separated by a deep valley (V-shaped) (figure 7.2).
Figure 7. Glossotherium robustum (1) upper left tooth series. Megatherium americanum (2) lower right tooth series / Glossotherium robustum (1) serie dentaria superior izquierda. Megatherium americanum (2) serie dentaria inferior derecha. Scale
bar / escala: 5 cm.
Shape analysis
RFTRA analysis consists of comparisons of skulls, in lateral and palatal views, and mandibles in lateral views of pair of specimens, i.e. L. armatus, M. darwini and S. leptocephalum compared with G. robustum as the base specimen. Table 1 shows the distance coefficients for each pair of comparisons.
Table 1. Morphological distances obtained through shape analysis
using RFTRA (Distance coefficients = D) / distancias morfológicas obtenidas a través del análisis de la forma usando RFTRA (coeficientes de distancia = D).
Glossotherium robustum - Lestodon armatus (figure 8). The overall shape of the skulls of G. robustum y L. armatus has the lowest morphological distance among the ground sloths included in this analysis, which indicates the highest similarity. The most relevant change is observed in the muzzle region. Lestodon armatus has the maxilla more lengthened in its mesial and ventral part, which becomes evident for the anterior displacement of the premaxillomaxillar suture. The caniniform is also anteriorly displaced, while the first molariform moves posteriorly, with the subsequent formation of a large diastema. The mandibles are also very similar. As in the skull, the most remarkable change is the anterior displacement of the caniniform and the longer diastema in L. armatus.
Figure 8. Results of RFTRA analysis on Glossotherium robustum - Lestodon armatus. Skulls (1) and mandibles (2) in lateral view,
and skulls in palatal view (3) / Resultados del análisis mediante RFTRA en Glossotherium robustum -Lestodon armatus. Cráneos (1) y mandíbulas (2) en vista lateral, y cráneos en vista palatal (3).
Glossotherium robustum - Mylodon darwini (figure 9). The morphological distance between G. robustum - M. darwini is greater than that observed between G. robustum - L. armatus. The most remarkable change is observed in the anterior part of the skulls. Mylodon darwini has the muzzle much more elongated, which is clear in lateral and palatal view. This is due to an enlargement of the premaxillae, maxillae and nasals. Mylodon darwini has the palate more convex at the level of M1, and the molariform series is posteriorly displaced. A generalized narrowness of the skull of M. darwini is observed in palatal view, and the tooth series are displaced to the middle line, becoming almost parallel. The shapes of the mandibles are similar even though in M. darwini is more slender and elongated in its anterior part than in G. robustum.
Figure 9. Results of RFTRA analysis on Glossotherium robustum - Mylodon darwini. Skulls (1) and mandibles (2) in lateral view, and
skulls in palatal view (3) / resultados del análisis mediante RFTRA en Glossotherium robustum -Mylodon darwini. Cráneos (1) y mandíbulas (2) en vista lateral, y cráneos en vista palatal (3).
Glossotherium robustum - Scelidotherium leptocephalum (figure 10). The skulls of these species show remarkable differences reflected in the morphologi- cal distance, which is even greater than those of the previous comparisons. The overall shape of the skull of S. leptocephalum is more slender than G. robustum. It is particularly more shallow, elongated and narrow, which is evident in lateral and palatal view. The enlargement of the skull is restricted to the muzzle region; the premaxillae and the nasals are notably lengthened. The tooth series are almost parallel and the molariforms are displaced posteriorly, which shortens the tooth series and lengthens the muzzle. The distance coefficients of the mandibles are lower than those of the skulls. The most notable changes in S. leptocephalum are the predental space more lengthened and narrow, the anterior part of the symphysis lower, the posterior displacement of the teeth and the condyle more elevated.
Figure 10. Results of RFTRA analysis on Glossotherium robustum- Scelidotherium leptcephalum. Skulls (1) and mandibles (2) in lateral
view, and skulls in palatal view (3) / Resultados del análisis mediante RFTRA en Glossotherium robustum-Scelidotherium leptocephalum. Cráneos (1) y mandíbulas (2) en vista lateral, y cráneos en vista palatal (3).
Glossotherium robustum-Megatherium americanum. These specimens show the highest distance coefficients (skull and mandible in lateral view) in relation with comparisons among mylodontids. Bargo (2001b: figure 7) described the most important changes: the snout of M. americanum is extended anteriorly and slightly depressed dorsoventrally; the basicranium is elevated well above the alveolar plane, and the braincase is shorter. The zygomatic process of the squamosal and the ascending process of the jugal lie further dorsally, while the tip of the descending process of the jugal lies at nearly the same level as in G. robustum. The molariform series is displaced posteriorly, leaving a long predental space. The angular, condylar and coronoid processes of the mandible are markedly displaced dorsally in M. americanum respect to G. robustum. The horizontal ramus, except at the well-developed ventral bulge, is shallower. The predental space is longer, due to the more distal tooth row.
Masticatory musculature
The origin and insertion areas of the masticatory
musculature in G. robustum, L. armatus, M. darwini
and S. leptocephalum do not differ markedly. They follow
the same pattern, showing minor variations in
the shape or roughness of the attachment areas.
M. temporalis. This muscle is usually divided into
superficial and deep portions in most living mammals
(Turnbull, 1970), including tree sloths. Naples
(1989) indicated that the m. temporalis was probably
undivided in Paramylodon harlani. In the mylodontid
ground sloths analyzed here, features in the
skull that might indicate divisions of the muscle are
ambiguous, thus the m. temporalis is recognized as a
unit. It aroses from the temporal fossa, which is
elongated, well defined, with a scarred surface, and
covered most of the dorsal and lateral parts of the
frontal and parietal bones. Mylodontids lack a
sagittal crest, but the dorsal origin of the muscle is
marked by the temporal line, which extends anteriorly
to the prominent postorbital processes, and
posteriorly nearly to the margins of the nuchal
crests. The m. temporalis inserted, probably tendinously
as in other mammals (Turnbull, 1970), on
the roughened lateral, anterior, and medial surfaces
of the coronoid process.
M. massetericus. The masseteric musculature is complex
in almost all mammals. It is usually subdivided
into superficial and deep components and the m. zygomaticomandibularis.
Although the m. massetericus superficialis
and m. massetericus profundus may be recognized,
the subdivisions of the m. m. superficialis cannot
be reliably reconstructed in mylodontids. The m.
m. superficialis arose laterally from the zygomatic
arch, as is indicated by the scarred central and lower
part of the descending process of the jugal, and inserted mainly on the lateral surface of the angular
process. The m. m. profundus presumably arose on a
smooth depression of the antero-medial surface of
the descending process of the jugal, and inserted on
the base of the coronoid process, anterodorsally to
the m. m. superficialis. The m. zygomaticomandibularis
was probably large in mylodontids. This is reflected
by the well developed and elongated ascending
process of the jugal. This muscle arose from the
scarred anteromedial surface of this process, and inserted
on the smooth depression of the masseteric
fossa at the base of the coronoid process, and above
the m. m. profundus.
M. pterygoideus. The pterygoid musculature in
sloths is large relative to that of other mammals (Edgeworth,
1935; Naples, 1985, 1989; Turnbull, 1970),
and is subdivided in the m. pterygoideus lateralis and
medialis, as typically occurs in other mammals. The
m. pterygoideus medialis arose from a depression in the
lateroventral surface of the elongated pterygoid
flange, and inserted on the concave and prominently
scarred medial surface of the large angular process.
The m. pterygoideus lateralis originated on the lateral
surface of the pterygoid, probably above the m. pterygoideus
medialis and inserted in a roughened depression
on the anteromedial edge of the mandibular
condyle.
Jaw mechanics
Bite force and velocity: estimation of moment arms.
The estimation of the moment arm of the masticatory
muscle's line of action allows the comparison of
the relative forces of the muscles and bite, and, more
significant, the analysis of the relation between bite
force and velocity, comparing the proportions of the
combined moment arms of the m. massetericus and m.
temporalis with those of the bite.
The moment arms of the m. massetericus (Mm), m.
temporalis (Mt), and bite (Mb) of Glossotherium robustum,
Lestodon armatus, Mylodon darwini, and Scelidotherium
leptocephalum were estimated, and compared
with those obtained previously by Bargo
(2001b) for Megatherium americanum (table 2a, b and
c). The values of the moment arms show little variation
among the different species. However, the figures
of the ratio of muscle moment/bite moment
(r.Mb), which provide a measure of the relative bite
force generated at different points along the tooth
row and the bite velocity, are remarkable.
Megatherium americanum has the highest values all
along the tooth row, while mylodontids have similar
values between them (table 2c). High ratios indicate
strong, rather than fast mandibular movements.
Hence, the masticatory apparatus of M.
americanum is designed to generate larger bite forces
than those of mylodontids. The means for the posterior
teeth (X1) and for the whole series (X2) provide
a comparative measure of the bite force generated
at the posterior part of the mandible and its total
bite force, respectively. Accordingly, mean values
indicate that M. americanum has the strongest
bite all along the molariform series (X2 = 1.26), and
especially at the posterior ones (X1= 1.43), while
mylodontids have a less powerful bite with little
variation among them.
Table 2.a, Moment arms of m. massetericus, calculated from the uppermost, middle and lowermost point of the origin area of the muscle.
Mm1 - Mm5: momemt arms of m. massetericus generated from five lines of action. X: mean. Values are in mm /a, Brazos de momento del m. massetericus, calculados a partir de los puntos más superior, medio y más inferior del área de origen del músculo. Mm1 - Mm5: brazos de momento del m. massetericus generados a partir de cinco líneas de acción. X: promedio. Los valores son en mm.
Table 2.b, Moment arms of m. temporalis, calculated from the
posteriormost (Mt1), middle (Mt2) and anteriormost (Mt3) points
of the origin area of the muscle. X: mean, Values are in mm / brazos de momento del m. temporalis, calculados desde los puntos mas posterior (Mt1), medio (Mt2) y más anterior (Mt3) del área de origen del músculo. X: promedio. Los valores son en mm.
Table 2.c, Summary of mean values of moment arms and ratios muscle/bite / resumen de los valores promedio obtenidos de los brazos de momento y las razones músculo/mordida.
Mandibular movements inferred from tooth wear
facets and striations. The analyses of tooth wear
facets and particularly the leading and trailing interfaces
between hard and soft dentines in Glossotherium
robustum suggest that the main mandibular movement
was produced in anteromedial direction.
Although striations are not abundant, some have
been observed in the hard dentine, and they support
this direction. This pattern coincides with that described
by Naples (1989) for the North American
ground sloth Paramylodon harlani. The wear facets observed
in Lestodon armatus and Mylodon darwini are
not as evident as those of G. robustum, but the few
striations observed would indicate that the main
mandibular movement was in anteromedial direction,
as in generalized recent mammals (Hiiemae,
1978). The teeth of S. leptocephalum do not show
tooth-tooth contact wear facets in the hard dentine,
nor does it show striations. Nevertheless, leading
and trailing interfaces were observed in some teeth,
having the same orientation as in G. robustum, which
would probably indicate the same direction during
the main mandibular movement.
The occlusal surfaces of the teeth of M. americanum
are completely different from those of mylodontids
(figure 7). The molariforms are bilophodont, that
is, they bear two prominent, sharp, and transversely
oriented lophs separated by a deep V-shaped valley.
This feature produced an interlocking occlusion: in
the upper teeth, mesial lophs occlude between two
successive lower teeth, while the distal lophs occlude
in the deep valleys enclosed by the anterior and posterior
lophs of the lower teeth. This type of occlusion
avoids the wear pattern described by Greaves (1973),
but generates tooth-tooth contact facets, predominantly
vertical and bearing clear striations, and
tooth-food-tooth contact facets (compression).
Discussion
Biomechanical and morphogeometrical evidence
It is generally accepted that a high mandibular
condyle improves the mechanical advantage of the
m. massetericus by increasing the moment arm of the
lines of action, as occurs in living ungulates
(Maynard Smith and Savage, 1959; Turnbull, 1970;
Greaves, 1980). Moreover, a high glenoid cavity distributes
the bite force uniformly along the tooth series,
which results advantageous in those herbivores
that process great amounts of food (Greaves, 1980;
Spencer, 1995).
In G. robustum, L. armatus, M. darwini and S. leptocephalum,
the cranio-mandibular joint (CMJ) lies at
the level of the tooth series, or little above it. So, a low
moment arm of the m. massetericus (Mm) should be
expected. However, the Mm is high, similar to the giant
armadillos (pampatheres) (Vizcaíno et al., 1998;
De Iuliis et al., 2000) which have the condyle elevated
well above the tooth row and share many features
with some living ungulates, in which the main masticatory
effort is generated by the m. massetericus. The
latter is also true for the ground sloths, where the m.
massetericus is more developed than the m. temporalis.
Therefore, it becomes evident that there is another
morphological arrangement in ground sloths that allows
keeping the Mm elevated. The mechanical advantage
would have been given by the great development
of the zygomatic arch, particularly the descending
process of the jugal, which elongates significantly
the lever of the m. massetericus.
On the contrary, M. americanum has the mandibular
condyle well elevated above the tooth series, but
the Mm is low and similar to mylodontids. As noted
by De Iuliis (1996), the angular process in M. americanum
has a more dorsal position, accompanying the
condyle, averting in this way a dramatic rearrangement
of the muscular attachment sites and force vectors.
Bargo (2001b: figure 7) corroborated through
shape analysis that both the condyle and the angular
process are elevated nearly to the same degree, compared
with the mandible of G. robustum, and the
same is true for the masseteric fossa. Consequently,
the estimated Mm is the same in both forms.
The moment arm of the m. temporalis (Mt) of mylodontids
is, as expected, lower than Mm, and similar
among the different species, and the same is true
for M. americanum (Bargo, 2001a).
The combined moment arm -i.e. ratio of muscle
moment (Mm +Mt) to bite moment (Mb)- provides a
relative measure of the effective bite force generated
by the musculature. In this way, large ratios indicate
forceful biting rather than rapid jaw movements.
Hence, the masticatory apparatuses of G. robustum, L.
armatus, M. darwini and S. leptocephalum, which have
lower ratios than M. americanum (see Table 2c), are
designed to generate lesser bite forces all along the
tooth row compared to the megatheriid. Moreover,
the tooth rows are displaced distally in M. americanum
compared with mylodontids, as demonstrated
by RFTRA analysis (Bargo 2001b), which result in
shorter moment arms for bite positions, throughout
the tooth row, which in turn increase the bite force.
Lestodon armatus shows the lowest value among my-
lodontids in the first tooth (caniniform), given that it
is markedly displaced anteriorly, suggesting less
force but high velocity.
Both, megatheriids and mylodontids, have a wide
articular condyle (more extended laterally than anteroposteriorly)
and slightly convex, and the glenoid
fossa shallowly concave. This arrangement would
have permitted considerable freedom of motion of
the mandible, both mediolateral and anteroposterior.
There is more evidence that complements the latter,
but allows two different interpretations for both
groups. The analysis of wear facets, the continuous
and discontinuous interfaces, and striations in mylodontids
indicate that the main masticatory movement
was in anteromedial direction. Moreover, the
anterior and posterior parts of the zygomatic arch are
not fused, nor in contact, which lesses its ability to
withstand the great forces generated by the antagonistic
actions of m. massetericus and m. pterigoideus
during lateral movements. This feature would indicate
that, even though existing, the lateral movements
were not very strong and continuous during
mastication. In the case of megatheriids, the particular
tooth morphology (i.e. interlocking occlusion,
bilophodonty) would be maintained by performing
essentially orthal movements, and this is confirmed
by the analysis of wear facets. Similarly, the zygomatic
arch is large and robust, and the anterior and
posterior parts may be in contact (even fused in aged
individuals, De Iuliis, 1996), unlike the mylodonts in
this study which have an incomplete arch. The stoutly
built zygomatic arch, particularly the great development
of descending process, leaves a narrow space
between it, the horizontal ramus and, in part, the ascending
ramus, suggesting a physical restriction to
lateral movements (Bargo, 2001b).
Hiiemae and Crompton (1985) summarized the
mechanical principles of tooth design in relation to
the nature of the food. They recognized three basic
patterns: A) a mortar and pestle system suitable to
crush hard and brittle (e.g., nuts) or turgid (e.g., fruit
pulp) food; B) blades to cut soft but tough food (e.g.,
muscle and skin); and C) a serial array of low profile
blades acting as a milling machine for tough and
fibrous food (e.g., grass). The first two patterns coincide
respectively with "routes" 1 and 2, and the third
with "routes" 3 and 4 of Janis and Fortelius (1988:
224-225). The teeth of ground sloths do not fit strictly
within any of these patterns, but can be assigned
to an intermediate situation. In mylodontids, the
teeth are oval or semi-oval and show different degrees
of lobation. The hard and soft dentine layers
results in differential wear, generating a concave occlusal
surface, comparable to pattern A of Hiiemae
and Crompton (1985). The outer hard dentine forms
sharp cusps that, during the masticatory movement
would act as cutting edges. The combination of this
morphology with the evidence that the direction of
the mandibular movement is mostly anteromedial,
indicates that mylodontid teeth would represent an
intermediate situation between Hiiemae and
Crompton's patterns A and C, i.e. for crushing and
grinding. According to Janis and Fortelius (1988),
moderately tough and abrasive food such as leaves
require reciprocal blades for comminution of food
items, a function which is accomplished by orthal
chewing with bilophodont teeth ("route" 2). The
dentition of Megatherium americanum represents a
battery of high lophs, with sharp, cutting edges, similar
to the dentition of tapirs and kangaroos. This
morphology would represent an intermediate condition
between Hiiemae and Crompton's patterns A
and B, i.e. mainly for cutting, and crushing. This
morphology does not rule out processing food with
similar physical properties (soft but tough, fleshy)
of animal source, like muscle or skin (Bargo, 2001b).
The morphogeometrical analysis demonstrated
that the most important localized changes occur in
the mandibles and the muzzles (the palatal region),
while the shape of the neurocranium was more conservative,
probably due to strong phylogenetic constraints.
The palatal region and mandibles can be better
interpreted in a functional context and, consequently,
would be more influenced by dietary adaptations
as it was proposed for armadillos (Vizcaíno
and Bargo, 1998).
Ecomorphological evidence
Mendoza et al., (2002) demonstrated that, at least
in ungulates, the adaptation to a given trophic niche
involves complex patterns of covariation among
many morphological characters of the skull and
mandible. The lack of living analogs for ground
sloths precludes performing extensive ecomorphological
analyses to establish unequivocal correlations
between feeding behavior and morphological variables.
However, some craniodental variables were
applied and demonstrated to be useful in explaining
differences in feeding behavior, as will be discussed
below.
As became evident from the previous section, the
two groups analyzed -Mylodontidae and Megatheriidae-
are morphofunctionally distinct from each
other in their masticatory apparatuses, but taxa within
each group are markedly similar to each other.
Recent ecomorphological analyses of these ground
sloths include three craniodental variables: hypsodonty
index, relative width and shape of the muzzle,
and dental occlusal surface area (OSA). Hypsodonty
index was standardized as depth of the
mandible, measured at the level of the third molariform
tooth, divided by length of the molariform
tooth row. The index of relative muzzle width was
calculated as the ratio between the palatal width,
measured as a mean of the anterior and posterior
width of the palate, and the maximum muzzle width
(MMW). Because the premaxillae are reduced in
sloths, the MMW is generally on the maxilla. Finally,
the OSA was estimated digitizing the outlines of the
teeth in occlusal view, in order to collect the surface
contour of each tooth; the area enclosed by these
points was calculated by a numerical integer approximation.
(see Bargo, De Iuliis and Vizcaíno, 2006;
Bargo, Toledo and Vizcaíno, 2006; Vizcaíno, Bargo
and Cassini, 2006 for further explanations). The results
of these studies offer relevant information that,
coupled with the morphological and biomechanical
evidence presented in this contribution, allows a paleobiological
interpretation on the dietary habits of
the ground sloths.
The masticatory apparatus of mylodontids was
not particularly suited for producing strong bite
forces during mastication, and the main masticatory
movement was anteromedial. This, in turn, suggests
that mylodonts were not well suited for extensive
oral food processing, and the main action was crushing
and, in less degree, grinding. In contrast, the
feeding apparatus of Megatherium americanum was
well designed for generating very strong, predominantly
orthal movements that were used mainly for
cutting rather than crushing and grinding.
The analysis of dental occlusal surface area (OSA)
in xenarthrans by Vizcaíno, Bargo and Cassini (2006)
supports these proposals. These authors found that
mylodontids have extremely low OSA values in comparison
with living herbivorous mammals of equivalent
body size, which also suggests that mylodonts
had poor food oral processing. This fact was probably
compensated with by high fermentation in the digestive
tract, or lower metabolic requirements, or a
combination of both. Surprisingly, the OSA value of M. americanum is the one expected, or even higher,
for a mammal of its size, and much larger than those
of mylodontids. It is clear then that M. americanum
was better suited for oral food processing in the oral
cavity, and most likely had a lower fermentation capacity
and/or higher metabolic requirements.
Bargo, Toledo and Vizcaíno (2006) analyzed the
relationship between dietary habits and shape and
width of the muzzle of the five species of ground
sloths considered here, and examined models of food
intake by reconstructing musculature and cartilages
of the muzzle. According to these authors, ground
sloths can be divided in two groups with different
feeding behaviours: wide-muzzled sloths (Glossotherium
robustum and Lestodon armatus) that were mostly
bulk-feeders (i.e. ingest great amounts of food with
each bite; probably roughage and grass eaters), and
narrow-muzzled sloths (Mylodon darwini, Scelidotherium
leptocephalum and Megatherium americanum)
that were mixed or selective feeders (i.e. select plants
or plant parts; grass and/or tree and shrubs foliage
eaters). The muscle reconstruction indicates that the
upper lip, formed by the m. incisivus superior, was
probably square-shaped and not prehensile in widemuzzled
sloths, as in the white rhinoceros, C. simum.
This fact, coupled with the absence of incisors, indicates
that G. robustum and L. armatus simply used the
upper lip coupled with the tongue to pull out grass
and herbaceous plants. Similarly, narrow-muzzled
sloths (M. darwini, S. leptocephalum and M. americanum)
had a thick, cone-shaped and prehensile upper
lip, useful for food intake as in the black rhinoceros,
Diceros bicornis Linnaeus, 1758, used to select
particular plants or plant parts (e.g. leaves and
twigs). It is worth noting that, following Mendoza and Palmqvist (2008), the white rhino is a typical
grazer but its muzzle is relatively narrower than in
many mixed feeders. One plausible hypothesis is
that in some cases it is the lip morphology what determines
functional muzzle width, supporting the
need to consider muscular anatomy to complete
these discussions (see Bargo, Toledo and Vizcaíno,
2006 and references therein).
Finally, the comparative study of hypsodonty in
Pleistocene ground sloths by Bargo, De Iuliis and
Vizcaíno (2006) suggests that differences in crown
height may be explained by a combination of variables
(rather than any single), including dietary
preferences (nature of food items), habitat (close or
open, temperate or tropical) and behavior (feeding
at ground level or higher, digging, etc.). Recently,
Mendoza and Palmqvist (2008) demonstrated that
high-crowned teeth represent an adaptation of ungulates
against tooth wear resulting from the airborne
grit and dust accumulated on the herbaceous
plants of open environments. But the absence of
enamel, which would make the teeth less durable
and subject to faster wear, must be considered as responsible
for much of the hypsodonty observed in
sloths, as well as in all xenarthrans, obscuring the interpretation
of the individual contribution of each
these variables (see Bargo, De Iuliis and Vizcaíno,
2006 for a discussion on this matter). Within mylodontids,
S. leptocephalum has the highest hypsodonty
index (HI), followed by M. darwini, while L.
armatus and G. robustum have the lowest indices. On
the other hand, M. americanum has the highest HI,
even when compared with other megatheriines (i.e.
Eremotherium Spillman, 1948 from northern South
America and North America, and other Megatherium
species from north central and north western South
America). We cannot determine the degree to which
higher hypsodonty values in megatheriids and mylodontids
correspond to feeding on abrasive grasses
rather than browsing on foliage, as has been done
for living ungulates (Janis, 1988; Solounias and
Dawson-Saunders, 1988), simply because we cannot
know the proportion of grass in their diet. However,
one obvious factor in explaining differences in hypsodonty
in ground sloths is the increased presence of
grit caused by environmental differences resulting
from geographic distribution, or environmental
change over time, or particular habits. For example,
the differences in hypsodonty between the megatheriines
E. laurillardi (Lund, 1842) and M. americanum
might be explained as adaptations to different environments,
as reflected by their geographical distributions
(see De Iuliis et al., 2000; Bargo, De Iuliis and
Vizcaíno, 2006). Differences in environment over
time, such as from closed to open, were apparently
important in North American Paramylodon (McDonald,
1995). Digging behavior in S. leptocephalum and
G. robustum, including but not limited to searching
for food, was demonstrated by morphologic and
biomechanical analyses of the limbs (Bargo et al.
2000; Vizcaíno et al., 2001). Also, the narrow-muzzled
sloths S. leptocephalum and M. darwini would
have used their stoutly built muzzles to root up for
searching for food. These particular habits must
have played a considerable role in shaping the dental
characteristics of these sloths. In each of those
cases, the important agent was the relative abundance
of abrasive soil particles.
Several discoveries of mummified remains and
dung of different ground sloths taxa, from South and
North America, have provided additional evidence
for the inference of their diets (McDonald and De
Iuliis, 2008). For instance, the dominant vegetation
identified from dung of Mylodon darwini, found in a
cave at Ultima Esperanza, in Southernmost
Patagonia, was grasses and sedges (Moore, 1978);
which in some way supports the morphological information
given here (low OSA values = low metabolic
requirements or low quality food; narrow-muzzled
= selective and mixed feeder) for that taxon. The
novel application of stable isotopes analyses in xenarthrans
(e.g. Coltrain et al., 2004; Kalthoff and
Tütken, 2007), or DNA analysis, will provide a better
understanding of the sloth's diet.
Conclusions
The results provided by this morphological and
biomechanical study, coupled with the ecomorphological
data, allow inferring different dietary habits
for the most common species of Pleistocene ground
sloths. Next, it is possible to infer a probable niche
differentiation among these species, given that they
inhabited within the same habitat.
Within mylodontids, Glossotherium robustum and
Lestodon armatus, the wide-muzzled sloths, were
most likely bulk-feeders. Their lips coupled with
the tongue were used to pull out grass and herbaceous
plants, which probably was the main dietary
item. Mylodon darwini and Scelidotherium leptocephalum,
the narrow-muzzled sloths, were mixed or selective-
feeders with a prehensile lip that was used
to select particular plants or plant parts. These
species could have also used their muzzles (as hogs)
to root up food items, such as roots and tubers. Mylodontids
have also clear adaptations to digging in
their forelimbs, using their claws to help searching
for food. The tooth design of mylodontids, in relation
to the nature of food, indicates that teeth were
mainly for crushing and grinding turgid and fibrous
items respectively.
Megatherium americanum was probably the most
selective feeder, with a prehensile lip very thick and
strong, and more developed than in the narrow-muzzled
mylodontids. This condition probably enabled
M. americanum to selectively feed on particular plants
(shrubs) or plant parts (leaves, twigs, fruits). The
dentition was designed mostly for cutting soft but
tough items which might include flesh, leaving open
the possibility of an omnivorous diet
The use of alternative methods (biomechanics,
morphogeometry and ecomorphology) to complement
the basic morphologic analysis of the masticatory
apparatus of forms that have no clear analogs,
demonstrates to be very insightful for the inferences
of dietary habits. However, as mentioned above, is
clear that more evidence (e.g., coprological, biogeochemical,
palynological) is required in order to reconstruct
a more accurate understanding of the feeding
behavior of these giant ground sloths.
Appendix 1. Acronyms and list of material / acrónimos y lista de material.
Acronyms
BM(NH): Natural History Museum, Londres, Inglaterra.
CN: Zoological Museum, Copenhagen, Denmark.
MACN: Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Buenos Aires, Argentina.
MLP: Museo de La Plata, La Plata, Argentina.
MMCIPAS: Museo Municipal y Centro de Investigaciones Paleontológicas de Salto, provincia de Buenos Aires, Argentina.
MMP: Museo Municipal de Ciencias Naturales "L. Scaglia", Mar del Plata, Argentina.
MNHN: Museo Nacional de Historia Natural de Montevideo, Uruguay.
MNHN-BOL: Museo Nacional de Historia Natural, La Paz, Bolivia.
MNHNP: Muséum National d'Histoire Naturelle, Paris, France.
MRSC: Museo Paleontológico Real de San Carlos "Armando Calcaterra", Colonia, Uruguay.List of materials
MYLODONTIDAE
Glossotherium robustum
MACN 1114. Complete skull with dentition. "Upper Pampean", unknown locality.
MACN 11074. Complete skull and right dentary. Lujanian, Arrecifes river, Buenos Aires Province, Argentina.
MACN 11769. Skull missing zygomatic arches and dentition. Pleistocene, Sauce Chico stream, Tornquist, Buenos Aires Province, Argentina.
MACN 12715. Skull missing dentition. "Upper pampean", Gorchs, F.C.S., Salado river, Buenos Aires Province, Argentina.
MLP 3-136. Complete skull, with jugals and premaxillae reconstructed. Figured by Lydekker (1894), Pl. XLVIII, figs. 1 y 1a y
Pl. XLIX, fig. 2. "Upper Pampean", unknown locality.
MLP 3-137. Skull, mandible (missing m2), and part of the skeleton. "Pampean", Olivera, Buenos Aires Province, Argentina.
MLP 3-138. Skull, mandible, and part of the skeleton missing left foot and lumbar vertebrae. Figured by Lydekker (1894), Pl. LI. "Upper pampean", San Antonio de Areco, Buenos Aires Province, Argentina.
MLP 3-139. Skull, right dentary and incomplete skeleton of a juvenile specimen. "Upper pampean", Olivera, Buenos Aires Province, Argentina.
MLP 3-140. Skull, mandible, and part of the skeleton. Figured by Lydekker (1894), Pl. XLIX, fig.1, Pl.L y Pl. LII, fig. 1. "Upper pampean", Río Luján, Olivera, Buenos Aires Province, Argentina.
MMCIPAS 1042/1043. Skull missing premaxillae and mandible. Pleistocene, Salto, Buenos Aires Province, Argentina.
MMP 1489-M. Skull missing jugals, caniniforms and right M1. Statigraphic provenance and locality unknown.
MMP 1490-M. Skull missing jugals and caniniforms; molariforms not well preserved. Statigraphy and locality unknown.
MNHN 1390. Skull missing premaxillae, jugals and dentition, except right M3. Pleistocene (Libertad Fm.), Arroyo Las Limetas, Conchillas, Colonia Department, Uruguay.
MRSC 920. Skull missing jugals. Pleistocene, Arroyo San Juan, Colonia Department, Uruguay.Lestodon armatus
MACN 10830. Skull and mandible. "Lower pampean", North of
Mar del Plata sea cliffs, Buenos Aires Province, Argentina.
MACN 11687. Skull of a juvenile specimen. "Pampean", Carcarañá river, Santa Fe Province, Argentina.
MLP 3-3. Skull with caniniforms and mandible with molariforms but missing caniniforms; incomplete skeleton but restored. Skull figured by Lydekker (1894), Pl. LIII, Figs. 1 y 1a. "Pampean", San Antonio de Areco, Buenos Aires Province, Argentina.
MLP 3-29. Skull and mandible partially restored. Jugals, left upper caniniform, right premaxilla, right m4 and left m2-4 are missing. Skull figured by Lydekker (1894), Pl. LIII, Fig. 2. "Pampean", unknown locality.
MLP 3-30. Skull and mandible partially restored. Right M2 and M4, and left m2 are missing. Caniniforms restored. "Pampean", unknown locality.
MRSC 807. Complete skull. Stratigraphy unknown, Colonia, Uruguay.
MRSC 1020. Skull and mandible. Stratigraphy unknown, Colonia, Uruguay.Mylodon darwini
BM(NH) M-16617 (ex RCS 472, ex RCS 3940). Holotype. Mandible with dentition; tip of the simphysis, coronoid, angular and condilar processes missing. Late Pleistocene, Punta Alta cliffs, Bahía Blanca, Buenos Aires Province, Argentina.
CN 43. Skull and nearly complete skeleton. Statigraphic provenance unknown, Buenos Aires Province, Argentina.
MACN 991. Right dentary with the molars partially restored. "Pampean", Río Salado, Buenos Aires Province, Argentina.
MACN 5980. Complete isolated premaxillae with part of the nasal arch. "Lower pampean", Miramar, Buenos Aires Province, Argentina.
MACN 11502. Incomplete left dentary (missing angular and coronoid processes, and part of the symphisis) with m2 and m4.
"Lower pampean"?, Río Carcarañá cliffs, Santa Fe Province, Argentina.
MACN 15348. Incomplete skull, restored in the dorsal part of the nasals, the nasal arch, the pterigoid blades and the jugals. "Lower pampean"?, Buenos Aires Province, Argentina.
MLP 3-122. Incomplete skull, with the nasal arch but missing dentition. Figured by Lydekker (1894), Pl. LIV. "Middle pampean", Buenos Aires Province, Argentina.
MLP 3-762a. Incomplete skull, with the nasal arch, jugals and dentition missing. "Upper pampean", Olavarría, Buenos Aires Province, Argentina.
MLP 3-763. Incomplete skull, with the nasal arch, jugals and dentition missing. "Upper pampean", Olavarría, Buenos Aires Province, Argentina.
MLP 3-764. Complete skull with dentition. Dorsal tip of the nasal arch mising. "Pampean", Olavarría, provincia de Buenos Aires, Argentina.
MLP 36-VIII-12-1. Incomplete skull without dentition. "Lower pampean", Estación Bunge, Buenos Aires Province, Argentina.
MMCIPAS 2458. Incomplete skull; zygomatich arches, premaxillae, anterior part of the nasals and dentition mising. Pleistocene, Salto, Buenos Aires Province, Argentina.
MNHN-BOL-V 006470. Skull very well preserved, but without dentition and right jugal. Pleistocene, Mojotorillo, Potosi Department, Bolivia.Scelidotherium leptocephalum
MLP 3-671. Skull and mandible and several limb bones. "Pampean", Olavarría, Buenos Aires Province, Argentina.
MLP 3-401. Skull and mandible and almost complete skeleton. "Pampean", Buenos Aires Province, Argentina.
MLP 3-420. Skull and mandible. "Upper Pampean", Buenos Aires Province, Argentina.
MMP 9-S. Skull of a juvenile specimen missing the zygomatic arches. Ensenadan, northeastern sea cliffs of Mar del Plata, Playa Santa Elena, Buenos Aires Province, Argentina.
MMP 31-S. Skull missing the zygomatic arches and the right molariforms. Sea cliffs of Camet, Mar del Plata, Buenos Aires Province, Argentina.
MMP 127-S. Skull missing zygomatic arches, mandible, atlas, ulna, radio and other limb bones. Lujanian (Cobo Fm.) 100 m North of Arroyo Santa Clara, Buenos Aires Province, Argentina.
MMP 157-S. Skull and mandible missing dentition. Playa Estrada, Mar del Plata, Buenos Aires Province, Argentina.
MMP 458-S. Skull and mandible. Skull mssing right M1, M4 and M5; mandible missing left m1- m4. Femur, patella, tibia, fragment of fibula and radio. Parque Camet, Mar del Plata, Buenos Aires Province, Argentina.
MMP 549-S. Skull, missing the zygomatic arches; mandible, with the coronoid processes and condyles incomplete. Part of the apendicular skeleton. Lujanian (Cobo Fm.), sea cliffs of Santa Clara del Mar, Buenos Aires Province, Argentina.
MMP 614-M. Skull missing the zygomatic arches and part of the skeleton. Rivera, Buenos Aires Province, Argentina.
MMP 1155-M. Skull missing the jugals, left M1-M5and right M3- M4; mandible missing dentition and right coronoid process incomplete. Ensenadan, Mar del Plata, Buenos Aires Province, Argentina.MEGATHERIIDAE
Megatherium americanum
MLP 2-64 Skull and mandible, with part of the hyoid apparatus. "Pampean", Argentina. Figured in Lydekker (1894: pl. 45, fig.1).
MLP 2-56. Complete mandible. "Pampean", Argentina. Figured in Lydekker (1894: pl. 45, fig. 1a).
MACN 1000, nearly complete mounted skeleton. Río Salado, Buenos Aires Province, Argentina.
MACN 2832. Skull and mandible, some hyoid pieces, vertebrae, fragment of scapula. "Pampean", Carcarañá river, Santa Fe, Argentina.
MACN 5002. Skull and mandible, femur, humerus and ulna. Palermo, Buenos Aires, Argentina. (Type of Megatherium gallardoi).
MNHNP 276. Skull and mandible with the symphysis broken. Stratigraphic provenance and locality unknown.
Appendix 2. Landmarks used for the morphogeometric analysis (H: homologous landmark; G: geometric landmark) / landmarksutilizados para el análisis morfogeométrico (H: landmarks homólogos; G: landmarks geométricos).
Skull: lateral view
1. Ventral margin of the occipital condyle (G).
2. Dorsal margin of the sagittal crest (H).
3. Parietofrontal suture on the sagittal plane (H).
4. Nasofrontal suture on the sagittal plane (H).
5. Anterior end of the nasal (G).
6. Nasointermaxillare (anterior end of the nasopremaxillar suture) (H).
7. Anterior end of the premaxilla (G).
8. Premaxillomaxillar suture on the ventral margin (H).
9. Mesial margin of first molariform tooth (H).
10. Mesial margin of second molariform tooth (H).
11. Distal margin of the last molariform tooth (H).
12. Ventral-most margin of the pterygoid (G).
13. Auditory foramen (H).
14. Squamoso-parieto-frontal suture (H)
15. Lacrimal foramen (H)
16. Infraorbital foramen (H)
17. Dorsal end of the ascending process of the jugal (G)
18. Ventral end of the descending process of the jugal (G)
19. Anterior end of the squamosal (G)Skull: palatal view
1. Posterior end of the right occipital condyle (G).
2. Posterior end of the left occipital condyle (G).
3. Left estilohyal fossa (H).
4. Rigth estilohyal fossa (H).
5. Palation (posterior point of the palate in the middle line) (H).
6. Anterior end of the right squamosal (G).
7. Anterior end of the left squamosal (G).
8. Rigth Infraorbital foramen (H).
9. Left Infraorbital foramen (H).
10. Premaxillomaxillar suture on the left margin (H).
11. Premaxillomaxillar suture on the middle line of the palate (H).
12. Premaxillomaxillar suture on the rigth margin (H).
13. Prosthion (anterior point of the premaxilla in the middle line) (H).
14. Mesial margin of first left molariform tooth (H).
15. Mesial margin of second left molariform tooth (H).
16. Mesial margin of the last left molariform tooth (H).
17. Mesial margin of first right molariform tooth (H).
18. Mesial margin of second right molariform tooth (H).
19. Mesial margin of the last right molariform tooth (H).Mandible: lateral view
1. Dorsal end of the condyle (G).
2. Junction between the condylar and coronoid processes (G).
3. Dorsal tip of the coronoid process (G).
4. Distal margin of the last molariform tooth (H).
5. Mesial margin of the second molariform tooth (H).
6. Mesial margin of the first molariform tooth (H).
7. Anterior symphyseal margin (G).
8. Intersection of the ventral margin of the dentary with the line extending down perpendicularly from the line drawn between landmarks 7 and 11 and at ¼ the distance between 7 and 11 (G).
9. Intersection of the ventral margin of the dentary with the line extending down perpendicularly from the line drawn between landmarks 7 and 11 and at ½ the distance between 7 and 11 (G).
10. Intersection of the ventral margin of the dentary with the line extending down perpendicularly from the line drawn between landmarks 7 and 11 and at ¾ the distance between 7 and 11 (G).
11. Posterior margin of angular process (G).
12. Junction between the angular process and the condyle (G).
13. External foramen of the dentary channel (H).
14. Anterior mental foramen (H).
Acknowledgments
MSB express her gratitude to her colleagues (S. Vizcaíno, G. De Iullis, R. Fariña and G. Cassini) and student N. Toledo for their valuable and enthusiastic contribution on this research. The authors acknowledge the following persons for the access to study the collections: R. Pascual and M. Reguero (Museo de La Plata), J. Bonaparte and A. Kramarz (Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Buenos Aires), A. Dondas (Museo Municipal de Ciencias Naturales "L. Scaglia", Mar del Plata), J. Ramírez (Museo Municipal de Salto, Buenos Aires Province), F. Anaya (Museo Nacional de Historia Natural, La Paz, Bolivia), A. Mones (Museo Nacional de Historia Natural de Montevideo, Uruguay), Mrs. Calcaterra (Museo Paleontológico Real de San Carlos "A. Calcaterra", Colonia, Uruguay). P. Christiansen for facilitating photographs of Mylodon darwini from the Museum of Copenhagen. Finally, we thank the reviewers H.G. McDonald and P. Palmqvist for his valuable comments and suggestions. This is a contribution to the projects PIP-CONICET 5240, PICT 26219 and UNLP N 474.
References
1. Ameghino F. 1889. Contribución al conocimiento de los mamíferos fósiles de la República Argentina. Actas de la Academia Nacional de Ciencias (Córdoba) 6: 1-1027.
2. Bargo, M.S. 2001a. [El aparato masticatorio de los perezosos terrestres (Xenarthra, Tardigrada) del Pleistoceno de la Argentina. Morfometría y biomecánica. Tesis Doctoral Universidad Nacional de La Plata, La Plata, Argentina. 400 pp. Unpublished.].
3. Bargo, M.S. 2001b. The ground sloth Megatherium americanum: skull shape, bite forces, and diet. Acta Paleontologica Polonica, Special Issue 46: 41-60.
4. Bargo, M.S. De Iuliis, G. andVizcaíno, S.F. 2006. Hypsodonty in Pleistocene ground sloths. Acta Paleontologica Polonica 51: 53- 61.
5. Bargo, M.S., Toledo, N. and Vizcaíno, S.F. 2006. Muzzle of South American ground sloths (Xenarthra, Tardigrada). Journal of Morphology 267: 248-263.
6. Bargo, M.S., Vizcaíno, S.F., Archuby, F.M. and Blanco R.E. 2000. Limb bone proportions, strength and digging in some Lujanian (Late Pleistocene-Early Holocene) mylodontid ground sloths (Mammalia, Xenarthra). Journal of Vertebrate Paleontology 20: 601-610.
7. Benson, R.H., Chapman, R.E. and Siegel, A.F. 1982. On the measurement of morphology and its change. Paleobiology 8: 328- 339.
8. Bookstein, F.L. 1981. Coordinate systems and morphogenesis. En: T.G. Connelly, L.L. Brinkley, and B.M. Carlson (eds.), Morphogenesis and Pattern Formation. Raven Press, New York, pp. 265-287.
9. Burchell, W.J. 1817. Note sur une nouvelle espèce de Rhinoceros (Rh. simus). Bulletin des Sciences, par la Société Philomatique: 96- 97.
10. Cabrera, A. 1926. Sobre la alimentación del megaterio. Boletín de la Real Sociedad Española de Historia Natural 26: 388-391.
11. Carlini, A.A. and Scillato-Yané, G.J. 2004. The oldest Megalonychidae (Xenarthra: Tardigrada); phylogenetic relationships and an emended diagnosis of the family. Neues Jarburch Für Geologie und Paläontologie Abhandlungen 233: 423- 443.
12. Chapman, R.E. 1990a. Conventional Procrustes approaches. En: F.J. Rohlf y F.L. Bookstein (eds.), Proceedings of the Michigan Morphometrics Workshop. Special Publication Nr. 2, University of Michigan, Ann Arbor, pp. 251-267.
13. Chapman, R.E. 1990b. Shape analysis in the study of dinosaur morphology. En: K. Carpenter y P.J. Currie (eds.), Dinosaur Systematics: Perspectives y Approaches. Cambridge University Press, pp. 21-42.
14. Chiarello, A.G. 2008. Sloth ecology: an overview of field studies. En: W.J. Loughry y S.F. Vizcaíno (eds.), The Biology of the Xenarthra, University Press of Florida, pp. 269-280.
15. Coltrain, J.B., Harris, J.M., Cerling, T.E., Ehleringer, J.R., Dearing, M.-D., Ward, J. and Allen, J. 2004. Rancho La Brea stable isotope biogeochemistry and its implications for the palaeoecology of late Pleistocene, coastal California. Palaeogeography, Palaeoclimatology, Palaeoecology 205: 199-219.
16. Costa, R.L. and Greaves, W.S. 1981. Experimentally produced tooth wear facets and the direction of jaw motion. Journal of Paleontology 55: 635-638.
17. Cuvier, G. 1796. Notice sur le squelette d'une très-grande espèce de quadrupède inconnue jusqu'à présent, trouvé au Paraquay, et déposé au cabinet d'histoire naturelle de Madrid. Magasin Encyclopèdique: ou Journal des Sciences, des Lettres et des Arts 1796, 1: 303-310; 1796, 2: 227-228.
18. De Iuliis, G. 1996. [A systematic review of the Megatheriinae (Mammalia: Xenarthra: Megatheriidae). PhD Dissertation University of Toronto, Canada. 719 pp. Unpublisehd.].
19. De Iuliis, G., Bargo, M.S. and Vizcaíno, S.F. 2000. Variation in skull morphology and mastication in the fossil giant armadillos Pampatherium spp. y allied genera (Mammalia: Xenarthra: Pampatheriidae), with comments on their systematics and distribution. Journal of Vertebrate Paleontology 20: 743-754.
20. Edgeworth, F.H. 1935. The cranial muscles of Vertebrates. Cambridge: Cambridge University Press, 493 pp.
21. Esteban, G. 1996. [Revisión de los Mylodontinae cuaternarios (Edentata, Tardigrada) de Argentina, Bolivia y Uruguay. Sistemática, Filogenia, Paleobiología, Paleozoogeografía y Paleoecología. Tesis Doctoral Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán. 235 pp. Unpublisehd.].
22. Fariña, R.A. 1985. Some functional aspects of mastication in Glyptodontidae (Mammalia). Fortschritte der Zoologie 30: 277-280.
23. Fariña, R.A. 1988. Observaciones adicionales sobre la biomecánica masticatoria en Glyptodontidae (Mammalia; Edentata). Boletín de la Sociedad Zoológica de Uruguay (2a. época) 4: 5-9.
24. Fariña, R.A. 1996. Trophic relationships among Lujanian mammals. Evolutionary Theory 11: 125-134.
25. Fariña, R.A. and Blanco, R.E. 1996. Megatherium, the stabber. Proceedings of the Royal Society of London 263: 1725-1729.
26. Fariña, R.A. and Vizcaíno, S.F. 2001. Carved teeth and strange jaws: How glyptodonts masticated. Acta Paleontologica Polonica, Special Issue 46: 87-102.
27. Ferigolo, J. 1985. Evolutionary trends of the histological pattern in the teeth of Edentata (Xenarthra). Archives Oral Biology 30: 71- 82.
28. Gaudin, T.J. 2004. Phylogenetic relationships among sloths (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. Zoological Journal of the Linnean Society 140: 255-305.
29. Gervais, P. 1855. Recherches sur les mammifères fossiles de l'' Amérique méridionale. Comptes Rendus de l' Académie des Sciences 40: 1112-1114.
30. Greaves, W. S. 1973. The inference of jaw motion from tooth wear facets. Journal of Paleontology 47: 1000-1001.
31. Greaves, W.S. 1978. The jaw lever system in ungulates: a new model. Journal of Zoology 184: 271-285.
32. Greaves, W.S. 1980. The mammalian jaw mechanism: the high glenoid cavity. The American Naturalist 116: 432-440.
33. Harlan, R. 1825. Fauna Americana: being a description of the mammiferous animals inhabiting North America. Philadelphia: Anthony Finley; J. Harding, pp. 199-203.
34. Hiiemae, K.M. 1978. Mammalian mastication: a review of the activity of the jaw muscles and the movements they produce in chewing. En: P.M. Butler y K.A. Joysey (eds.), Development, function and evolution of teeth, Academic Press, London, pp. 359-398.
35. Hiiemae, K.M. and Crompton, A.W. 1985. Mastication, food transport, and swallowing. En: M. Hildebrand, D.M. Bramble, K.F. Liem y D.B. Wake (eds.), Functional Vertebrate Morphology, Harvard University Press, Cambridge and London, pp. 262- 290.
36. Hofmann, R.R. and Stewart, D.R.M. 1972. Grazer or browser: a classification based on the stomach structure and feeding habits of East African ruminants. Mammalia 36: 226-240.
37. Illiger, C. 1811. Prodromus systematis mammalium et avium additis terminis zoographicis utriusque classis. C. Salfeld, Berolini, 301 pp.
38. Janis, C.M.. 1995. Correlations between craniodental morphology and feeding behavior in ungulates: reciprocal illumination between living and fossil taxa. En: J. Thomason (ed.), Functional Morphology in Vertebrate Palaeontology, Cambridge University Press, pp. 76-98.
39. Janis, C.M. 1988. An estimation of tooth volume and hypsodonty indices in Ungulate mammals, and the correlation of these factors with dietary preference. En: D.E. Russell, J.P. Santoro y D. Sigogneau-Russell (eds.), Teeth revisited: Proceedings of the VII International Symposium on Dental Morphology, Memoirs de Musée national d'Histoire naturelle (serie C) 53: 367-387.
40. Janis, C.M. and Ehrhardt, D. 1988. Correlation of the muzzle width and relative incisor width with dietary preference in ungulates. Zoological Journal of the Linnean Society 92: 267-284.
41. Janis, C.M. and Fortelius, M. 1988. On the means whereby mammals achieve increased functional durability of their dentitions, with special reference to limiting factors. Biological Review 63: 197-230.
42. Kalthoff, D. and Tütken, 2007. Stable isotope composition of extant xenarthran teeth and their potencial fr the reconstruction of the diet of fosil xenarthrans (Mammalia). 8º International Congress of Vertebrate Morphology (Paris), Abstracts: 62.
43. Kraglievich, L. 1922. Estudio sobre los Mylodontinae. Análisis comparado de los valores craneométricos de los milodontinos de Norte y Sud América. Anales del Museo Nacional de Historia Natural de Buenos Aires 31: 457-464.
44. Kraglievich, L. 1923. Descripción comparada de los cráneos de Scelidodon rothi Ameghino y Scelidotherium parodii n. sp. Anales del Museo Nacional de Historia Natural de Buenos Aires 33: 57- 103.
45. Kraglievich, L. 1928. "Mylodon darwini" Owen es la especie genotipo de "Mylodon" Owen. Rectificación de la nomenclatura genérica de los milodontes. Physis 9: 169-185.
46. Kraglievich, L. 1934. Contribución al conocimiento de Mylodon darwini Owen y especies afines. Revista del Museo de La Plata 34: 255-292.
47. Lydekker, R. 1886. Description of three species of Scelidotherium. Proceedings of the Zoological Society of London: 496-497.
48. Lydekker, R. 1894. Contributions to a knowledge of the fossil vertebrates of Argentina, Part II: The extinct edentates of Argentina. Anales del Museo de La Plata (Paleontología Argentina) 3: 1-118.
49. Linnaeus, C. 1758. Systema Naturae per regna tria naturae, secundum classis, ordines, genera, species cum characteribus, differentiis, synonymis, locis. Laurentii Salvii, Stockholm, 824 pp.
50. Lund, P.W. 1842. Blik paa Brasiliens Dyreverden for Sidste Jordomvaeltning. Fjerde Afhandling: Fortsaettelse af Pattedyrene. Detkongelige Danske Videnskabernes Selskabs Skrifter. Naturvidenskabelige og Mathematisk Afhandlinger 9: 137-208.
51. Macalister, A. 1869. On the myology of Bradypus tridactylus; with remarks on the general anatomy of the Edentata. Annual Magazine of Natural History 4: 51-67.
52. Maynard Smith, J. and Savage, R.J.G. 1959. The mechanics of mammalian jaws. School Sciences Review 141: 289-301.
53. McDonald, H.G. 1987. [A systematic review of the Plio-Pleistocene scelidothere ground sloths (Mammalia: Xenarthra, Mylodontidae). PhD Dissertation, University of Toronto, Toronto. 478 pp. Unpublished.].
54. McDonald, H.G. 1995. Gravigrade Xenarthrans from the early Pleistocene Leisey Shell Pit 1A, Hillsborough County, Florida. Bulletin of Florida Museum of Natural History 37: 345-373.
55. McDonald, H.G. and De Iuliis, G. 2008. Fossil history of sloths. En: W.J. Loughry y S.F. Vizcaíno (eds.), The Biology of the Xenarthra, University Press of Florida, pp. 39-55.
56. Mendoza, M. and Palmqvist, P. 2008. Hypsodonty in ungulates: an adaptation for grass consumption or for foraging in open habitat? Journal of Zoology 274: 134-142.
57. Mendoza, M., Janis, C. and Palmqvist, P. 2002. Characterizing complex craniodental patterns related to feeding behavior in ungulates: a multivariate approach. Journal of Zoology London 258: 223-246.
58. Merino, M.L., Milne, N. and Vizcaíno, S.F. 2005. A morphometric study of deer (Mammalia, Cervidae) crania from Argentina using three dimensional landmarks. Acta Theriologica 50: 91- 108.
59. Moore, D.M. 1978. Post-glacial vegetation in the south Patagonian territory of the giant ground sloth, Mylodon. Botanical Journal of the Linnaean Society 77: 177-202.
60. Moore, W.J. 1981. The Mammalian Skull. Cambridge University Press, 369 pp.
61. Naples, V.L. 1982. Cranial osteology and function in the tree sloths, Bradypus and Choloepus. American Museum Novitates 2739: 1-41.
62. Naples, V.L. 1985. Form and function of the masticatory musculature in the tree sloths, Bradypus and Choloepus. Journal of Morphology 183: 25-50.
63. Naples, V.L. 1987. Reconstruction of cranial morphology and analysis of function in the Pleistocene ground sloth Nothrotheriops shastense (Mammalia, Megatheriidae). Contributions in Science, Los Angeles County Museum of Natural History 389: 1-21.
64. Naples, V.L. 1989. The feeding mechanism in the Pleistocene ground sloth, Glossotherium. Contributions in Science, Los Angeles County Museum of Natural History 415: 1-23.
65. Owen, R. 1839. Fossil Mammalia (2). En: C.R. Darwin (ed.), The Zoology of the Voyage of the M.S.H. Beagle, London, 1(7): 41-64.
66. Owen, R. 1840. Fossil Mammalia (4). En: C.R. Darwin (ed.), The Zoology of the Voyage of the M.S.H. Beagle, London, 1(13): 81- 111.
67. Owen, R. 1842. Description of the skeleton of an extinct gigantic sloth, Mylodon robustus, Owen, with observations on the osteology, natural affinities, and probable habits of the megatherioid quadruped in general. R. and J. E. Taylor, London, 176 pp.
68. Owen, R. 1843. Letter from Richard Owen, Esq., F.R.S., F.G.S. etc., etc., on Dr. Harlan's notice of new fossil Mammalia. American Journal of Sciences and Arts 44: 341-345.
69. Owen R. 1856. On the Megatherium (Megatherium americanum Cuvier and Blumenbach). III. The skull. Philosophical Transactions of the Royal Society of London 146: 571-589.
70. Owen R. 1857. On the Scelidothere (Scelidotherium leptocephalum) Owen. Philosophical Transactions of the Royal Society of London 147: 101-110.
71. Owen, R. 1860. Memoir on the Megatherium or Giant Ground-Sloth of America (Megatherium americanum, Cuvier). Taylor y Francis, London, 84 pp.
72. Plotnick, R. and Baumiller, T.K. 2000. Invention by evolution: functional analysis in paleobiology. En: D.H. Erwin y S.L. Wing (eds.), Deep Time. Paleobiology's perspective. Supplement to Paleobiology 26: 305-321.
73. Pérez, L.M., Scillato-Yané, G.J. and Vizcaíno, S.F. 2000. Estudio morfofuncional del aparato hioideo de Glyptodon sp. (Cingulata, Glyptodontidae). Ameghiniana 37: 293-299.
74. Rensberger, J.M. 1973. An occlusion model for mastication and dental wear in herbivorous mammals. Journal of Paleontology 47: 515-528.
75. Scillato-Yané, G.J. 1977. Octomylodontinae: nueva subfamilia de Mylodontidae (Edentata,Tardigrada). Descripción del cráneo y mandíbula de Octomylodon robertoscagliai n.sp., procedentes de la formación Arroyo Chasicó (Edad Chasiquense, Plioceno temprano) del sur de la Provincia de Buenos Aires (Argentina). Algunas consideraciones filogenéticas y sistemáticas sobre los Mylodontoidea. Publicaciones del Museo Municipal de Ciencias Naturales de Mar del Plata L. Scaglia 2: 123-140.
76. Scillato-Yané, G.J. 1986. Los Xenarthra fósiles de Argentina (Mammalia, Edentata). 4º Congreso Argentino de Paleontología y Bioestratigrafía (Mendoza), Actas 2: 151-165.
77. Sicher, H. 1944. Masticatory apparatus of the sloths. Fieldiana: Zoology 29:161-168.
78. Sinclair, W.J. 1905. New Mammalia from the Quaternary caves of California. University of California Publications, Bulletin of the Department of Geology 4: 145-161.
79. Smith, K.K. 1993.The form of the feeding apparatus in terrestrial vertebrates: studies of adaptation and constraint. En: J. Hanken y B.K. Hall (eds.), The skull, volume 3: Functional y Evolutionary mechanisms. The University of Chicago Press, Chicago y London, pp. 150-196.
80. Solounias, N. and Dawson-Saunders, B. 1988. Dietary adaptations and palaeoecology of the late Miocene ruminants from Pikermi and Samos in Greece. Palaeogeography, Palaeoclimatology, Palaeoecology 65: 149-172.
81. Solounias, N. and Moelleken, S.M. 1993. Dietary adaptation of some extinct ruminants determined by premaxillary shape. Journal of Mammalogy 74: 1059-1071.
82. Solounias, N., Teaford, M. and Walker, A. 1988. Interpreting the diet of extinct ruminants: the case of a non-browsing giraffid. Paleobiology 14: 287-300.
83. Spencer, L.M. 1995. Morphological correlates of dietary resource partitioning in the African Bovidae. Journal of Mammalogy 76: 448-471.
84. Spillman, F. 1948. Beiträge zur Kenntnis eines neuen gravigraden Riesensteppentieres (Eremotherium carolinense gen. et spec. nov.), seines Lebensraumes und seiner Lebensweise. Paleobiologica 8: 231-279.
85. Stock, C. 1925. Cenozoic gravigrade edentates of Western North America with special reference to the Pleistocene Megalonychinae and Mylodontidae of Rancho La Brea. Carnegie Institution of Washington Publications 331: 1-206.
86. Turnbull, W.D. 1970. Mammalian masticatory apparatus. Fieldiana Geology 18: 149-356.
87. Turnbull, W.D. 1976. Restoration of masticatory musculature of Thylacosmylus. En: C.S. Churcher (ed.), Essays on Palaeontology in Honour of Loris Shano Russel, Athlon, Royal Ontario Museum Life Sciences Miscellaneous Publication, pp. 169-185.
88. Vizcaíno, S.F. 1994. Mecánica masticatoria de Stegotherium tessellatum Ameghino (Mammalia, Xenarthra) del Mioceno temprano de Santa Cruz (Argentina). Algunos aspectos paleoecológicos relacionados. Ameghiniana 31: 283-290.
89. Vizcaíno, S.F. 2000.Vegetation partitioning among Lujanian (late Pleistocene-early Holocene) armored herbivores in the pampean region. Current Research in the Pleistocene 17: 135-137.
90. Vizcaíno, S.F. and Bargo, M.S. 1998. The masticatory apparatus of Eutatus (Mammalia, Cingulata) and some allied genera. Evolution y paleobiology. Paleobiology 24: 371-383.
91. Vizcaíno, S.F. and De Iuliis, G. 2003. Evidence for advanced carnivory in fossil armadillos (Mammalia: Xenarthra: Dasypodidae). Paleobiology 29: 123-138.
92. Vizcaíno, S.F. and Fariña, R.A. 1997. Diet and locomotion of the armadillo Peltephilus: a new view. Lethaia 30: 79-86.
93. Vizcaíno, S.F., De Iuliis, G. and Bargo, M.S. 1998. Skull shape, masticatory apparatus, and diet of Vassallia y Holmesina (Mammalia: Xenarthra: Pampatheriidae). When anatomy constrains destiny. Journal of Mammalian Evolution 5: 291-322.
94. Vizcaíno, S.F., Bargo, M.S. and Cassini, G.H. 2006. Dental occlusal surface area in relation to body mass, food habits and other biologic features in fossil Xenarthrans. Ameghiniana 43: 11-26.
95. Vizcaíno, S.F., Zárate, M., Bargo, M.S. and Dondas, A. 2001. Pleistocene large burrows in the Mar del Plata area (Buenos Aires Province, Argentina) and their probable builders. Acta Paleontologica Polonica, Special Issue 46: 157-169
96. Vizcaíno, S.F., M.S. Bargo, R.F. Kay and N. Milne. 2006. The armadillos (Mammalia, Xenarthra) of the Santa Cruz Formation (early-middle Miocene). An approach to their paleobioloy. Palaeogeography, Palaeoclimatology, Palaeoecology 237: 255-269.
97. Webb, S.D. 1985. The interrelationships of tree sloths y ground sloths. En: G.G. Montgomery (ed.), The Evolution y Ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington, pp. 105-112.
98. White, J.L. 1997. Locomotor adaptations in Miocene Xenarthrans. En: R.F. Kay, R.H. Madden, R.L. Cifelli, y J.J. Flynn (eds.), Vertebrate Paleontology in the Neotropics. The Miocene Fauna of La Venta, Colombia, Smithsonian Institution Press, 16: 246-264.
99. Windle, B.C.A. and Parsons, F.G. 1899. On the myology of Edentata. Proceedings of the Zoological Society of London 1: 314- 339.
100. Winge, H. 1941. Edentates (Edentata). En: S. Jensen, R. Spärck y H. Volsoe (eds.), The Interrelationships of the Mammalia genera, Reitzels Forlag, Copenhagen, pp. 319-341.
Recibido: 22 de agosto de 2006.
Aceptado: 4 de diciembre de 2007.