Dental occlusal surface area in relation to body mass, food habits and other biological features in fossil xenarthrans
Sergio F. Vizcaíno 1 , M. Susana Bargo 1 and Guillermo H. Cassini 2
1 Departamento Científico Paleontología de Vertebrados, Museo de La
Plata, Paseo del Bosque s/n, 1900 La Plata, Argentina. CONICET-CIC. vizcaino@museo.fcnym.unlp.edu.ar,
msbargo@museo.fcnym.unlp.edu.ar
2 Departamento de Ciencias Básicas, Universidad Nacional de
Luján, Rutas 5 y 7, 6700 Luján, Argentina. ghnanca@yahoo.com.ar
Abstract. The Xenarthra includes the most intriguing mammals from the Cenozoic of South America: the glyptodonts (Cingulata) and the ground sloths (Tardigrada). Their masticatory apparatuses are diverse and peculiar, with a strongly reduced, hypselodont dentition that lacks enamel and displays different degrees of lobation. The goal of this study is to investigate the relationship between dental occlusal surface area (OSA) and diet, and other physiological factors in fossil xenarthrans. Over one hundred and fifty specimens, including living herbivorous epitherians and both extinct and living xenarthrans, were measured and photographed, and their OSA estimated and plotted against body mass. For most fossil xenarthrans OSA is smaller than expected for extant herbivorous mammals of equivalent body size. Within xenarthrans, cingulates show the highest OSA values, suggesting more extensive oral food processing than in tardigrades. Among ground sloths, mylodontids have extremely low OSA values, suggesting low efficiency in oral food processing that was probably compensated by high fermentation in the digestive tract, or lower metabolic requirements, or a combination of both adaptations. On the other hand, Megatherium americanum has an OSA expected for, or even higher than that of, a mammal of its size, which indicates higher oral food processing, lower fermentation capacity, and/or higher metabolic requirements.
Resumen. Área de la superficie oclusal dentaria en relación con la masa corporal, hábitos alimenticios y otros rasgos biológicos en Xenartros fósiles. El grupo de los Xenarthra incluye los mamíferos más intrigantes del Cenozoico de América del Sur: los gliptodontes (Cingulata) y los perezosos terrestres (Tardigrada). Sus aparatos masticatorios son diversos y peculiares, con una dentición fuertemente reducida, hipselodonte, que carece de esmalte y presenta distintos grados de lobulación. El objetivo de este trabajo es investigar la relación que existe entre el área de la superficie oclusal dentaria (OSA), la dieta y otros factores fisiológicos en xenartros fósiles. Se midieron y fotografiaron más de ciento cincuenta especímenes, que incluyen epiterios herbívoros actuales y xenartros vivientes y fósiles; se estimaron sus OSAs y graficaron contra la masa corporal. Para la mayoría de los xenartros fósiles la OSA es menor que la esperada para mamíferos herbívoros vivientes de tamaño corporal equivalente. Dentro de los xenartros, los cingulados arrojan los valores mayores de OSA, lo que sugiere un procesamiento del alimento en la cavidad oral más extensivo que en los tardigrados. Entre los perezosos terrestres, los milodóntidos presentan valores de OSA extremadamente bajos, lo que indica una baja eficiencia en el procesamiento oral del alimento, que podría compensarse con una alta fermentación en el tracto digestivo o con requerimientos metabólicos menores, o una combinación de ambas adaptaciones. Por otra parte, Megatherium americanum posee la OSA esperada para un mamífero de tamaño equivalente, o inclusive mayor, lo que sugiere un mayor procesamiento oral del alimento, menor capacidad de fermentación y/o mayores requerimientos metabólicos.
Key
words. Mammalia; Xenarthra; Dental Occlusal Surface Area; Body mass; Diet; Physiology.
Palabras clave. Mammalia; Xenarthra; Área de la Superficie Oclusal
Dentaria; Masa corporal; Dieta; Fisiología.
Introduction
The Order Xenarthra represents one of the four major clades of placental mammals (Murphy et al ., 2001; Madsen et al ., 2001; Delsuc et al ., 2003). The other three, Afroteria, Euarchontoglires and Laurasitheria, were previously believed to be a single clade, Epitheria (McKenna, 1975). Within xenathrans, glyptodonts and ground sloths are, without doubt, the most intriguing South American Cenozoic mammals. The former (Suborder Cingulata) are armoured animals related to the living armadillos while the latter (Suborder Tardigrada) are related to the living tree sloths. The masticatory apparatuses of cingulates and tardigrades are truly diverse and peculiar. The dentition is strongly reduced: armadillos and glyptodonts usually have no incisors or canines and nine or ten cheek teeth in each quadrant, while sloths usually have four or five. All living xenarthrans, and possibly all extinct ones, lack enamel in the adult, deciduous dentitions except Dasypus Linné and the cuspal pattern observed in other mammals. Teeth are always hypselodont ( i.e ., high-crowned and evergrowing) and, although they can be lobate, are usually simple and separated by short spaces (figure 1).
Figure 1. Upper left tooth series of
different fossil xenarthrans / series dentarias izquierdas superiores de
distintos xenartros fósiles. A, Eutatus seguini (Dasypodidae),
B, Holmesina occidentalis (Pampatheriidae), C, Panochthus
tuberculatus (Glyptodontidae), D, Glossotherium robustum (Mylodontidae),
E, Megatherium americanum (Megatheriidae). Scale bar = 5 cm /
Escala = 5 cm.
Morpho-functional analyses
of the masticatory apparatus of fossil xenarthrans, including biomechanical and
morpho-geometric methods, have been performed recently as a basis for the
interpretation of their dietary adaptations. These studies include dasypodid
armadillos (Vizcaíno and Fariña, 1997; Vizcaíno and Bargo, 1998; Vizcaíno and
De Iuliis, 2003), pampatheriid armadillos (Vizcaíno et al ., 1998; De
Iuliis et al ., 2000), glyptodonts (Fariña, 1985,1988; Fariña and
Vizcaíno, 2001) and ground sloths (Bargo, 2001a and 2001b).
At the same time, much research has focused on relationships between aspects of
mammalian dental morphology ( i.e ., size, shape and wear) and trophic
characterizations. Understanding these relationships allows inferences on
feeding adaptations from the teeth of fossil forms (Ungar and Williamson,
2000). Most of this research has been carried out in extant and extinct
herbivorous ungulates (Fortelius, 1985; Janis, 1988, 1990, 1995; Spencer, 1995;
Fortelius and Solounias, 2000; Pérez-Barbería and Gordon, 1998, 2001; Williams
and Kay, 2001; Mendoza et al ., 2002) and primates (see Kay and Ungar,
1997 and references therein).
Although the xenarthran
dental peculiarities mentioned above reflect some phylogenetic constraints
(Vizcaíno and De Iuliis, 2003) that should be considered (see Discussion), it
is possible to quantify and compare some of these variables within xenarthrans,
using the “form-function correlation approach" noted by Radinsky (1987). This
approach assumes that a close relation exists between form and function, so
that the latter can be predicted from the former. Such investigations have
benefited greatly when combined with knowledge of closely related taxa. In the
absence of suitable homologies, the tendency has been to argue for function
based on analogy, usually biological. Moreover, when biological analogues are
not available, mechanical ones have often been used (see Plotnick and
Baumiller, 2000, for an extensive discussion on this matter).
Janis (1995) demonstrated that some craniodental variables allow discrimination
among ungulates of grazing, browsing and mixed feeding habits (but see,
Pérez-Barbería and Gordon, 2001 for an alternative interpretation with a
different methodological approach). Several authors (Janis, 1990, 1995; Janis
and Constable, 1993; Mendoza et al ., 2002) have noted that the
cheek-teeth occlusal surface area (OSA) is larger in grazers than in browsers
among ungulates and kangaroos. For instance, Janis (1988, 1995) stated that
monogastric ungulates, such as perissodactyls, have longer molarized premolar
rows than ruminant artiodactyls. Janis and Constable (1993) and Janis (1995)
proposed that these differences are due to different alimentary strategies in
relation with differences in the physiology of digestion. Horses in comparison
with cows (ruminants) spend more time chewing and they also chew more when they
eat food with a high fiber content.
The purpose of this paper is to investigate the relationships among cheek-teeth
( i.e ., molariforms) occlusal surface area, body mass, inferred diet,
and other biological factors in different fossil xenarthrans. These results
provide insightful information that, together with the above-mentioned studies,
will allow the development of reasonable interpretations of their dietary
behaviour.
Material and methods
For the purpose of this
paper, more than one hundred and fifty specimens from collections housed in
different museums were measured (see Appendix 1). The data base includes
forty-seven species of living, mostly herbivorous, epitherian mammals of very
different sizes of the orders Rodentia, Hyracoidea, Tubulidentata, Proboscidea,
Artiodactyla, and Perissodactyla, and twenty-four species of Xenarthra,
including ten fossil and four living Cingulata and seven fossil and three
living Tardigrada.
The fossil tardigrades and cingulates analysed include most of the Pleistocene
species that have been previously studied (see above). As these were
specialized forms of great size (from approximately 800 to 5000 kg; Fariña et
al ., 1998; Bargo et al ., 2000), several older species (Miocene and
Pliocene in age) with lower body masses were included to widen the sample. The
sloth taxa include Glossotherium robustum (Owen), Lestodon armatus Gervais,
Mylodon darwini Owen, and Scelidotherium leptocephalum Owen
(Mylodontidae), Hapalops sp. Ameghino and Megatherium americanum Cuvier
(Megatherioidea), and Eucholoeops sp. Ameghino (Megalonychidae). The
cingulates include Propalaeohoplophorus australis Ameghino, Propalaeohoplophorus
incisivus Ameghino, Asterostemma depressa Ameghino, Plohophorus sp.
Ameghino, Panochthus tuberculatus Burmeister, Glyptodon sp. Owen
(Glyptodontidae), Holmesina occidentalis (Hoffstetter) (Pampatheriidae)
and Eutatus seguini Gervais (Dasypodidae).
Usually, cheek-teeth OSA has been measured indirectly by multiplying the width
and length of molars and premolars in some ungulates ( e.g ., Janis,
1988, 1995; Pérez-Barbería and Gordon, 1998, 2001), which have nearly
quadrangular teeth. This simple method does not consider infolding of the
enamel, fossae, cusps and lophs. Hence it would be not suitable for many xenarthrans
such as the glyptodonts and mylodontids with their lobated molariforms and the
bilophodont molariforms of megatheres which require a different technical
approach. Since the relationships between OSA and the three-dimensional surface
of the tooth are unknown for different tooth types (Pérez-Barbería and Gordon,
1998), for this paper we will approach this problem considering OSA as the
two-dimensional projection of a three-dimensional structure. Digital photos of
the occlusal surfaces of the upper cheek tooth rows were taken, including
molars and premolars in epitherians and molariforms in xenarthrans. The choice
of the upper cheek teeth for this analysis was due to limitations in the
availability of material, especially among fossil specimens. The OSA of teeth
depends on the individual history or age ( i.e ., old individuals have a
greater OSA than juveniles, Pérez-Barbería and Gordon, 1998). In order to avoid
these differences, all specimens included in this analysis were adults.
Therefore, adults with highly worn teeth ( i.e ., little or no enamel
left on the occlusal surface) and juveniles ( i.e. , animals in which
the last molar is not erupted) were excluded. These considerations are
irrelevant for xenarthrans, since they lack enamel and have ever-growing teeth,
so that OSA does not vary much with age in adults.
The outlines of the teeth were digitized in palatal view using WinDIG 2.5
software ( http://www.unige.ch- /cpb/windig.html ). For each individual a set of xi
, yi coordinate pairs describing the surface contour of each tooth
was collected, and the area enclosed by these points was calculated by
Simpson's numerical integer approximation. This method is frequently used in
continental aquatic ecology to calculate the surface area of irregular lakes or
lagoons (Dangavs, 1995). OSA is the sum of the area of each tooth in the
series.
The OSA values obtained were plotted against body mass. For living species,
when body mass was not available in museum records it was estimated from 3 to 5
cranial and/or postcranial allometric equations for each specimen, depending on
the completeness of the material, and excluding dental measurements (Janis,
1990; Biknevicius et al ., 1993). The values obtained were reasonably within
the range for adult specimens reported in the literature (Redford and
Eisenberg, 1989; Nowak, 1991). Given the strikingly peculiar design of the
skulls, jaws, teeth and limbs of fossil xenarthrans, and the absence of proper
analogues among living members of the clade, body mass estimations should be
approached cautiously (see Vizcaíno and De Iuliis, 2003, for an extensive
discussion on the phylogenetic constraints of the group). In this study, body
masses were obtained from the best estimators taken from Fariña et al .
(1998) and Bargo et al . (2000). In these articles the mass of fossil
xenarthrans were estimated from regression equations adjusted in modern
ungulates with craniodental and postcranial variables, and the averages
obtained were contrasted with estimates obtained from scale and geometric
models. In the few cases for which the available skeletal elements were
insufficiently complete, geometric similarity with a phylogenetically close
relative with an appropriate estimation was assumed.
The two variables (OSA and body mass) were log-transformed to convert the
relationship of these variables from an exponential function (Y=aWb) to a
straight linear function (LogY=log a + b logW) and reduce heteroscedasticity ( i.e
., the dispersion associated with high values) of the data (see Peters,
1983).
Regression lines, with log OSA taken as dependent variable and log body mass as
independent variable, were calculated by least squares method independently for
all extant mammals, living epitherians, and living and extinct xenarthrans.
Additionally, they were also calculated for various subgroups within
epitherians and xenarthrans, as follows:
1. Rodents (South American
hystricomorphs), 8 species.
2. Perissodactyls plus hyracoids (Families Equidae, Tapiridae,
Rhinocerotidae and Procaviidae), 17 species.
3. Artiodactyls (Families Antilocapridae, Cervidae, Bovidae, Giraffidae,
Camelidae and Hippopotamidae), 18 species.
4. Ruminant artiodactyls (Families Antilocapridae, Cervidae, Bovidae),
12 species.
5. Cingulates (Families Dasypodidae, Glyptodontidae and Pampatheriidae),
14 species.
6. Dasypodids, 5 species.
7. Glyptodontids, 8 species.
8. Tardigrades (Families Bradypodidae, Megatheriidae and Mylodontidae),
10 species.
Perissodactyls and hyracoids are lumped together, following Janis (1990), based on the convergence of dental morphology and digestive physiology in the two groups. All regression slopes were tested for isometry ( i.e ., if the calculated slope differs significantly from the expected value of 0.67) and for the expected scaling of metabolic requirements with mass ( i.e ., 0.75, as described by Kleiber´s law) by Student's t statistic (two-tailed test). Following Bell (1989), differences among groups, that is Epitherians vs. Xenarthrans and within xenarthran taxa, were studied by means of analyses of covariance (ANCOVA), using the log-transformed body mass as a covariable. The distributions around the regression line of different physiological or taxonomic groups were studied by means of a residual analysis. The residuals of each group were compared by means of the Mann-Whitney U test, which is the most powerful (or sensitive) non-parametric alternative to the t-test for independent samples. All statistical analyses were performed using the program Statistica (StatSoft, 1996).
Results
Appendix 1 lists the body
mass and the OSA for each specimen studied, and Appendix 2 lists the statistics
of both features for each species. Note that when compared with epitherians of
similar body size (for instance living xenarthrans against hyracoids and
rodents, or mylodontid fossil sloths against rhinos, hippos and elephants),
xenarthrans have smaller OSA. Also, it can be seen that within the largest
xenarthrans, ground sloths have smaller OSA values than the cingulates.
ANCOVA results show that the three pairs of comparisons (epitherians vs
xenarthrans, perissodactyls plus hyracoids vs ruminants, and cingulates vs
tardigrades) do not differ significantly (p = 0.05) in their adjusted values
for slopes (table 1). In the first case, the OSA values of xenarthrans are
significantly smaller than in epitherians of similar body mass (p < 0.0001);
in the second, the ruminants have significantly smaller OSA values than
perissodactyls of similar body mass (p < 0.0001); and in the last
comparison, the OSA values of tardigrades are significantly smaller than in
cingulates of similar body mass (p < 0.001).
Table 1. Results of ANCOVA for
comparisons between taxa listed of log-transformed data of occlusal surface
area, using the log-transformed body mass as covariable. Assumptions violating
test of parallelism are also presented. Significant
differences between groups are indicated by an asterisk / análisis de
covarianza de la comparación entre los taxones listados de los datos de área de
superficie oclusal transformados a logaritmo usando la masa corporal
transformada a logaritmo como covariable. También se presentan los resultados
del test de paralelismo. Las diferencias significativas entre los grupos están
indicadas por un asterisco.
Figure 2 shows the relationships between OSA and body mass for living mammals. Specimens belonging to different orders and/or families are identified by different symbols. This regression clearly shows that living xenarthrans that fall below the adjusted line have smaller OSA values than those expected for mammals of their size. In addition, it is clear how the different groups of taxa tend to cluster above or below the line: most rodents, hyracoids, proboscideans, perissodactyls (especially horses) fall above the regression line, while most artiodactyls (especially ruminants) fall below the regression line.
Figure 2. Regression of OSA against body
mass for living mammals (n = 125). Symbols: open triangles = Dasypodidae; black
triangles = Bradypodidae; gray triangle = Tubulidentata; black circles =
Caviomorpha; open circles = Hyracoidea; open squares = Tapiridae; gray squares
= Equidae; black squares = Rhinocerotidae; gray diamonds = Cervidae; open
diamonds = Bovidae; black diamonds = Giraffidae; gray circle = Hippopotamidae;
crosses = Camelidae; gray cross within square = Elephantidae. Dashed lines above and below the regression line = 95
% confidence interval / Regresión de las áreas de las superficies oclusales
dentarias (OSA) contra la masa corporal en mamíferos vivientes (n = 125).
Símbolos: triángulos en blanco = Dasypodidae; triángulos negros = Bradypodidae;
triángulos grises = Tubulidentata; círculos negros = Caviomorpha; círculos en
blanco = Hyracoidea; cuadrados en blanco = Tapiridae; cuadrados grises =
Equidae; cuadrados negros = Rhinocerotidae; rombos grises = Cervidae; rombos en
blanco = Bovidae; rombos negros = Giraffidae; círculos grises = Hippopotamidae;
cruces = Camelidae; cruces grises dentro de un cuadrado = Elephantidae. Líneas
punteadas por encima y por debajo de la línea de regresión = intervalo de
confianza del 95%.
Figure 3 compares independent regressions of epitherians and all xenarthrans (including fossils). Both regression lines seem to be parallel and the slopes do not differ significantly (p=0.05; see table 1). The taxa distributions of epitherians around the regression line do not show marked differences with the distribution observed for all living mammals regression in figure 2. The regression line of epitherians lies above that of xenarthrans. Among the latter, there are two taxa from different clades that are outliers: the pampatheriid cingulate Holmesina occidentalis and the giant ground sloth Megatherium americanum . Both lie well above the xenarthran regression line, falling on the line of epitherians. It is also remarkable that the mylodontid ground sloths fall well below the regression line for xenarthrans.
Figure 3 . Regression of OSA against
body mass of Xenarthra (n = 53) compared with Epitheria (n = 99). Symbols:
circles = Epitheria; black triangles = Xenarthra; E = Epitheria regression
line; X = Xenarthra regression line. Dashed lines above and below the
regression line = 95 % confidence interval. The black triangles contained by
the ellipse correspond to the mylodontid ground sloths. a. case of the
Pampatheriidae Holmesina . b. two cases of Megatherium ./ regresión
de las áreas de las superficies oclusales dentarias (OSA) contra la masa corporal
de Xenarthra (n = 53) comparado con Epitheria (n = 99). Símbolos: círculos = Epitheria; triángulos negros =
Xenarthra; E = línea de regresión de Epitheria; X = línea de regresión de
Xenarthra. Líneas punteadas por encima y por debajo de la línea de regresión =
intervalo de confianza del 95 %. Los triángulos negros dentro de la elipse
corresponden a los milodóntidos. a. caso del Pampatheriidae Holmesina . b. dos casos de Megatherium .
Figure 4 includes independent regressions for cingulates and tardigrades. The regression of cingulates lies above that of tardigrades, and has a higher, although not statistically different (p = 0.05), slope (table 1). The tardigrade regression clearly shows a differential distribution of some groups, which parallels that of figure 3. Mylodontids fall below the line, while M. americanum lies far above the regression line, being an outlier due to a great value of OSA (and not to a measuring error). When regression parameters are recalculated without M. americanum , the values adjusted for the slope become smaller ( i.e ., 0.52), compared to the value provided in table 2 for tardigrades (see below). The living sloths overlap both regression lines and do not show any particular distribution. In contrast, the cingulates are distributed tightly around the regression line, with the exception of H. occidentalis , which lies well above the line.
Figure 4. Regression of OSA against body
mass of xenarthrans (n = 53). Symbols: C = Cingulata; T = Tardigrada; black
triangles = dasypodid cingulates; gray triangle = pampatheriid cingulate; open
triangles = glyptodontid cingulates; open circles = living tardigrades; gray
circle = Eucholoeops ; open squares = Hapalops ; black squares = Megatherium
; black circles = mylodontids. Dashed
lines above and below the regression line = 95% confidence interval / regresión
de las áreas de las superficies oclusales dentarias (OSA) contra la masa
corporal de Xenarthra (n = 53). Símbolos: C = Cingulata; T = Tardigrada;
triángulos negros = cingulados dasipódidos; triángulos grises = cingulados
pampateridos; triángulos en blanco = cingulados gliptodóntidos; círculos en
blanco = tardigrados vivientes; círculos grises = Eucholoeops ;
cuadrados en blanco = Hapalops ; cuadrados negros = Megatherium ;
círculos negros = mylodontids. Líneas punteadas por encima y por debajo de la
línea de regresión = intervalo de confianza del 95%.
Table 2. Results of simple linear
regression for each group. The more common parameters, R-square value and
estimators of regression coefficients in bold. Differences between the values
adjusted for the slopes and that expected for isometry (2/3) were not
significant in all groups at p-level of 0.05 except for that tagged by an
asterisk (p = 0.01). Differences between the values adjusted for the slopes and
that expected for Kleiber´s law (0.75) were not significant only in groups
tagged by an asterisk (p = 0.01) or two asterisks (p = 0.05). Residual analysis
results are present when a pair of comparisons was statistically significant (p
< 0.01). Labels : E = Epitheria, X =
Xenarthra, P = Perissodactyla, A = Artiodactyla, C = Cingulata, T = Tardigrada,
Eq = Equidae, Tp = Tapiridae / resultados de las regresiones lineares
simples de cada grupo. Los parámetros más comunes, valor R-cuadrado y los
estimadores de los coeficientes de regresión están marcados en negrita. Las
diferencias entre los valores ajustados para las pendientes y aquellos
esperados para isometría (2/3) fueron no significativos para todos los grupos
(p = 0.05), excepto por aquél marcado con un asterisco (p = 0.01). Las
diferencias entre los valores ajustados para las pendientes y aquel esperado
para la ley de Kleiber (0.75) fueron no significativos solamente en los grupos
marcados con un asterisco (p = 0.01) o dos asteriscos (p = 0.05). Los
resultados del análisis de residuos fueron presentados cuando el par de
comparaciones fue estadísticamente significativo (p < 0.01). Leyendas: E =
Epitheria, X = Xenarthra, P = Perissodactyla, A = Artiodactyla, C = Cingulata,
T = Tardigrada, Eq = Equidae, Tp = Tapiridae.
The parameters for the regression lines in figures 2, 3 and 4, and some subgroups, are summarised in table 2. For all cases the R2 values obtained are greater than 0.9, indicating a high correlation between OSA and body mass. According to the t-test, all slopes do not differ significantly from the expected value for isometric relationship ( i.e ., 0.67 for a log relation between area and volume) in each case considered. This indicates that they would be parallel, in correspondence with parallelism test results. In all groups except for the perissodactyls plus hyracoids, dasypodids and glyptodontids (table 2), the t-tests allow us to conclude with 99% confidence, that the values adjusted for the slopes differ from that expected from Kleiber´s law ( i.e ., a 0.75 slope). Only in the three mentioned groups are the values adjusted for the slopes not significantly different from the two null hypothesis models ( i.e ., 0.67 and 0.75). In dasypodids and glyptodontids values for the two models for the slope are included in a wide confidence interval due to the small sample available. The graphic distributions of different groups around the regression line are statistically significant and supported by the residual analyses. In the regression line for living mammals, epitherians have greater OSA values than living xenathrans; in the epitherian regression line perissodactyls have greater OSA values than artiodactyls; for the xenarthran regression line (including living and fossil taxa) the residual analyses, as well as the ANCOVA, indicates that the cingulates have greater OSA values than tardigrades; and for the perissodactyls plus hyracoid regression line, residual analyses shows that equids have greater OSA values than tapirs.
Discussion
When structures differ in
size but have the same proportion, they are said to be isometric, and their
areas scale with mass to the power 2/3 (or 0.67). In biology isometry usually
exists only for limited size ranges within single species, for instance insects
and arachnids (Prange, 1977) and lizards (McMahon and Bonner, 1983). For larger
ranges, proportions change with size and that change is described as
allometric. For our general sample of mammals, which includes a large range of
body sizes, OSA increases with mass by the power 0.70, which, according with
the Student's t-test results (see Table 2 to review the two null hypothesis),
suggests isometry.
This is particularly evident in the slope of Epitheria (0.66). Within
ungulates, the artiodactyls (especially the ruminant artiodactyls) are
distributed below the regression line with lower OSA values, while the
monogastric forms lie above the regression line, which indicates that their OSA
values are larger than expected for their body size. This is in accordance with
Janis' (1988, 1995) conclusion that the monogastric ungulates, such as the
perissodactyls, have longer and more molarized premolar rows than ruminants;
and the molars of the former are also bigger and more quadrangular than in the
latter. Following Janis and Constable (1993) and Janis (1995), this difference
is due to different alimentary strategies reflecting differences in the
physiology of digestion. Horses chew their food more than ruminants during the
first stages of ingestion and, in contrast to the latter, chew more when the
proportion of fiber in the food increases. Within the perissodactyls, the
equids, which are mainly grazers and live in open habitats, have greater OSAs
than tapirs, which are browsers and live in more closed habitats. Similarly,
within artiodactyls, mixed feeding or grazing bovids and camelids have larger
OSAs than browsing cervids and giraffids. This suggests that in ungulates
chewing area is also related to the nutritional value of food: browsers consume
succulent leaves while grazers ingest forage that is of lower quality and
highly abrasive for teeth. Additionally, within ruminants Texera (1974)
observed that subadult individuals of the cervid Hippocamelus Leuckart
spent more time chewing than adults, a behaviour attributed to the smaller OSA
of subadults due to unerupted third molars. A remarkable case is the
hippopotamus. Its teeth are unusually small for such a large grazing mammal, a
condition probably related to its low metabolic rate (Owen-Smith, 1988). The
preceding examples indicate that OSA may thus be correlated with the capacity
to process food in the oral cavity and, indirectly, with some aspects of
feeding physiology and metabolism.
Xenarthrans have less OSA available for triturating food than epitherians of
similar sizes. This fact may be related to the low basal metabolic rates
characteristic of living xenarthrans, which fall between 40 and 60 percent of
the rates expected from mass in Kleiber's (1932) relation for placental mammals
(McNab, 1985). This implies that xenarthrans have less energetic requirements
than epitherians and, therefore, for a specific type of food, require lower
intakes than epitherians of similar body masses.
Within xenarthrans, cingulates have the highest OSA values, suggesting a
greater oral cavity food processing than in tardigrades. It is interesting to
note that large herbivorous cingulates, such as pampatheres and glyptodonts,
have lobated teeth. Feeding behaviour in these forms was postulated as ranging
from browsing to grazing (Vizcaíno et al ., 1998; De Iuliis et al .,
2000; Fariña and Vizcaíno, 2001). Tooth lobation is more complex in glyptodonts
than in pampatheres, producing more extensive shearing edges for food
processing. Moreover, a glyptodont tooth is highly hypselodont and bears a
longitudinal osteodentine (compact dentine) crest and, in each lobe, a
transverse crest. This morphology, coupled with other morphometric features of
their skulls and jaws, led Fariña and Vizcaíno (2001) to place them near the
group of grazers in the graphs presented by Janis (1990). In the case of
pampatheres, tooth lobation is less complex, but OSA is much larger. It seems
probable that, in some way, a reduction in one feature is compensated for by an
increase in the other. Holmesina occidentalis , with its high OSA, also
lacks the hard osteodentine crest, indicating another aspect to consider with
respect to compensation. In general, pampatheres seem to have higher OSAs and
fewer ridges and less shearing surfaces. Although there is no direct evidence
of the rate of metabolism of pampatheres and glyptodonts, indirect evidence,
such as the pattern of geographic distribution in North America, indicates that
their northern limit were restricted by the combination of low metabolism and
high thermal conductance (McNab, 1985). Also, there may be a relationship
between the OSA and stomach morphology that may help to explain why cingulates
fall above the regression line compared to tardigrades. Modern armadillos have
a simple sac-like stomach (Grassé, 1955) compared to living sloths with a
chambered stomach (Britton, 1941) so presumably do not have the same level of
digestive efficiency. Cingulates like glyptodonts and pampatheres probably also
had a simple sac-like stomach that lacked chambers and therefore would need a
more complex dental apparatus, i.e., lobate teeth and greater OSA to better
process vegetation than sloths. Among sloths, the extremely low OSA values for
mylodontids might reflect poor food oral processing abilities. If this were the
case these ground sloths, in order to maintain diets similar to those of the
ungulates of equal body masses, would have been expected to compensate for the
low efficiency in food processing with high fermentation capability in the
digestive tract, and/or lower metabolic requirements. The living tree sloths, Bradypus
Linné and Choloepus Illiger, have an extremely large four-chambered
stomach and so presumably this is also true for all fossil sloths. Food passage
through the digestive tract is very slow (up to one week) and, consequently,
the digestion and absorption rhythm is also extremely slow (Britton, 1941).
Moreover, the generally slow nature of tree sloths, due to the poor skeletal
musculature, also implies lower metabolic requirements than in other mammals
(Scholander, 1955; McNab, 1985). Naples (1989) assumed that Glossotherium also
had a slow rate of passage of food through the gut, which might have enabled
this sloth to obtain sufficient nutrition from high fiber foods. If the
presumed chambered stomach of mylodontids was a functional equivalent to the
chambered stomach of ruminants, then in both groups digestion in the stomach is
an important component that allows a more efficient extraction of nutrients and
permits a smaller OSA. Consequently, it could be argued that the smaller OSA in
mylodontids indicates increased digestive efficiency and a longer transit time
in the gut that permitted a more efficient absorption of nutrients. As a
consequence there may not be as strong selection for the oral mechanical
processing of vegetation. Small OSA may also in part be a reflection of the low
metabolism, as occurs in the hippopotamus, which has a complex three chambered
stomach, relatively small teeth, a restricted rate of food intake and a
relatively low metabolic rate (Owen-Smith, 1988); and individuals have been
known to survive for many weeks in a mud wallow without food, water, or shade
(Nowak, 1991).
Surprisingly, Megatherium americanum has an expected, or even higher,
OSA value for a mammal of its size, and a much larger OSA value than expected
compared with mylodontids, which may represent a high specialization for the
former. Following Janis (1995), if a parallel with ungulates is assumed,
mylodontids might be inferred as foregut fermenters, while M. americanum would
have been a hindgut fermenter, which in turn reflect lower and higher quality
nutritional diets, respectively (Alexander, 1996). However, the absence of a
caecum in living xenarthrans might indicate that M. americanum was not a
hindgut fermenter. In this case the great difference in OSA values between M.
americanum and mylodontids might suggest that the former had less developed
chambers (in number and/or size) than the latter. While stomach anatomy, except
in a few exceptional cases, cannot be compared among fossil taxa, it is clear
that M. americanum was better suited for food processing in the oral
cavity than were mylodontids. This is in accordance with other morphological
and biomechanical evidence discussed extensively by Bargo (2001a). The teeth of
M. americanum are extremely hypselodont and bilophodont, with the
sagittal section of each loph being triangular and sharp-edged (figure 1). This
occlusal morphology indicates that the way OSA has been calculated in this
study does not reflect the sum of the total area present on the anterior and
posterior surfaces of the two lophs.
From a functional point of view, the morphology described above suggests that
the teeth were well adapted for strong, predominantly orthal movements and were
used mainly for cutting rather than crushing and grinding (Bargo, 2001a). We do
not know yet how much one function is enhanced over the other, or how much one
complements the other.
The evidence provided by Bargo (2001a) indicates that M. americanum could
have fed on moderate to soft tough food, probably browsing (including fruits)
in open habitats, and the possibility that it was capable of processing flesh
cannot be excluded (Fariña, 1996; Fariña and Blanco, 1996). Fruits and flesh
are food items nutritionally richer than most grasses or leaves; richer diets
require smaller fermentation chambers (Alexander, 1996) and strict carnivores
do not have chambers at all. Frugivory and carnivory imply that flesh and fruit
eaters presumably do not require the same degree of mastication, and then the
larger OSA in Megatherium may have been an indirect way of enlarging the
cutting area, since cutting does not result in the breakage of cell walls and
the release of nutrients as efficiently as crushing and grinding does.
Additionally, OSA is assumed to be directly correlated with the quantity of
food trapped between the upper and lower tooth rows. Hence, in species with
strong jaw muscles which crush their food between sets of interlocking
cheek-teeth, as is the case in Megatherium , a large OSA is functionally
important (Pérez-Barbería and Gordon, 1998 and references therein), increasing
the amount of food fragments cut or ground per chewing cycle.
The great OSA of M. americanum would also suggest a basal metabolic rate
similar to that of an extant herbivorous mammal of equal body size. If M.
Americanum had a digestive tract as efficient for processing cellulose as
mylodonts, it would have been capable of maintaining a higher basal metabolism
compared to mylodonts. The ground sloths, in general, would have had low
metabolic rates, due to their large body masses (McNab, 1985; Naples, 1989),
probably lower than those ungulates of equivalent size. The skeletal
musculature, in contrast to living sloths, was well developed, given their
totally terrestrial locomotory habits, and some mylodontids ( i.e ., G.
robustum and S. leptocephalum ) were well adapted for digging
burrows (Bargo et al ., 2000; Vizcaíno et al ., 2001). This
adaptation would probably indicate an even lower basal metabolism for these
sloths compared with that for Megatherium americanum . McNab (1979,
1985) found that in armadillos low metabolic rates correlate with burrowing
habits, probably as a mean to reduce heat storage during this activity, which
would be even more important for the large burrowing ground sloths.
Finally, it is worth remembering that the absence in xenarthrans of many dental
specializations characteristic of advanced epitherians is most probably due to
biomechanical (Mendoza et al ., 2002) and phylogenetic constraints
(Vizcaíno and De Iuliis, 2003). Several authors (Winge, 1941; Hirschfeld and
Webb, 1968; Patterson and Pascual, 1972; Hirschfeld, 1976; Webb, 1985; Naples,
1987) have proposed that specializations for insectivory among early
xenarthrans imposed a severe constraint in the subsequent adaptations to
different diets among the various clades. From their earliest records,
xenarthrans are known to have possessed a homodont, hypselodont dentition that lacked
enamel, which would be a singularly derived condition for epitherians. Given
the early loss of enamel and the typical tribosphenic molar, we should not
expect xenarthrans to have evolved morphological responses convergent on those
of many epitherians. Specific biomechanical and morphofunctional analyses
provide more accurate reconstructions of these unusual extinct creatures than
straightforward, traditional comparisons with modern closely allied taxa or
supposed analogs, which alone can lead to misleading conclusions (Vizcaíno and
De Iuliis, 2003).
Acknowledgments
The authors would like to thank F. Momo, P. Palmqvist, G. De Iuliis and G. McDonald for their comments and valuable input on the manuscript. To J. Cuisin (Laboratoire Zoologie Mammifères et Oiseaux) and F. Renourt (Laboratoire d'Anatomie Comparée) of the Muséum National d'Histoire Naturelle, Paris, A. Kramarz of the Museo Argentino de Ciencias Naturales “Bernardino Rivadavia", Buenos Aires, and M. Merino of the Mammalogy Collection of Museo de La Plata, Argentina, for allowing access to specimens in their care. This paper is a contribution to the projects Agencia Nacional de Promoción Científica y Tecnológica PICT 07-06348, Universidad Nacional de La Plata N-336.
Appendix 1. (Table3). Acronyms and list of the material used with their catalogue numbers, the estimated body masses in kg and the oclussal surface area (OSA) in mm2 of each specimen. / Acrónimos y lista de materiales utilizados con sus números de catálogo, masas corporales estimadas en Kg y superficies oclusales dentarias (OSA) en mm 2 de cada espécimen .
Appendix 2. (Table 4). Figures (means and standard
deviations) of dental occlusal surface area (OSA) in mm2 and estimated body
masses (in kg) for each species studied / valores (promedios y desvíos
standard) de las áreas de las superficies occlusales dentarias (OSA) en mm2 y
masas corporales estimadas (en kg) para cada especie estudiada.
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Recibido:
20
de abril de 2004.
Aceptado: 17 de febrero de 2005.