Young Darwin and the ecology and extinction of pleistocene south american fossil mammals
Sergio F. Vizcaíno1, Richard A. Fariña2 and Juan Carlos Fernicola3
1 División Paleontología Vertebrados, Museo de La Plata, La Plata, Argentina. CONICET. Email: vizcaino@fcnym.unlp.edu.ar
2 Departamento de Paleontología, Facultad de Ciencias, Universidad de la República, Montevideo. Uruguay. Email: fari~a@fcien.edu.uy
3 Sección Paleontología de Vertebrados, Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Buenos Aires. Argentina.
Email: jctano@macn.gov.ar
ABSTRACT
During his two years in South America Charles Darwin became fascinated not only with the lush vegetation of Brazil, but also with the gigantic Pleistocene mammals that he found in the drier areas of Uruguay, and in the pampas and Patagonian coast of Argentina. These findings included various ground sloths and glyptodonts among xenarthrans, and hoofed herbivores like Toxodon and Macrauchenia, in addition to horses and small rodents. He concluded that the general assumption that large animals require luxuriant vegetation was false and that vitiated the reasoning of geologists on some aspects of Earth's history. He also reflected on the evident changes that occurred in the continent, the extinct fauna of which suggested to him an analogy to southern parts of Africa. He wondered about our ignorance of biological traits in extinct creatures and the reasons for their extinction. Thus, not only did Darwin inspire phylogenetic studies on fossil mammal lineages, he also opened a gate to the research on their behaviour, physiology and extinction; i.e., their palaeobiology. Whereas the first approach was largely developed in South America beginning about the second half of the 19th century due to the intellectual influence of Florentino Ameghino, palaeobiology became a much more recent line of work, in apparent relation to innovations in methodology and technology. This contribution provides an overview of recent contributions on the palaeobiology of Pleistocene fossil mammals of South America as attempts to provide answers for Darwin's questions.
Keywords: Darwin; Ecology; Extinction; South America; Mammals.
RESUMEN: El joven Darwin y la ecología y extinción de los mamíferos fósiles sudamericanos. Durante los dos años que Charles Darwin estuvo en América del Sur no sólo se deslumbró con la profusa vegetación de Brasil, si no también con los gigantescos mamíferos pleistocenos que colectó en áreas más secas de Uruguay y en la pampa y la costa patagónica de Argentina. Sus hallazgos incluyeron distintos perezosos y gliptodontes, ungulados herbívoros como Toxodon y Macrauchenia, además de caballos y pequeños roedores. Darwin, desechó la presunción general de que los grandes animales requieren una exuberante vegetación, reconociendo que la misma condicionó las interpretaciones que hicieran los geólogos sobre algunos aspectos de la historia de la Tierra. También reflexionó sobre los cambios acaecidos en el continente, cuya fauna le sugirió una clara analogía con lo observado en el sur de África. Darwin se preguntó acerca de nuestro desconocimiento de las características biológicas y de las causas que llevaron a su extinción. Así, no sólo inspiró el estudio filogenético de distintos linajes de mamíferos fósiles, si no que abrió la puerta a las investigaciones sobre su comportamiento, fisiología y extinción; i.e. su paleobiología. En América del Sur, la influencia intelectual de Florentino Ameghino permitió apuntalar el estudio filogenético de los mamíferos durante la segunda mitad del Siglo XIX, mientras que el fortalecimiento de la paleobiología se dio en tiempos recientes en relación con innovaciones metodológicas y tecnológicas. Esta contribución provee una visión global de las contribuciones realizadas en paleobiología de mamíferos pleistocenos de América del Sur como un intento de responder los cuestionamientos que se hiciera Darwin.
Palabras clave: Darwin; Ecología; Extinción; América del Sur; Mamíferos.
INTRODUCTION
When HMS Beagle reached the coast of
Brazil in February, 1832, Charles Darwin
was a 22-year old theology student at
Cambridge University and his ambition
was to become a rural pastor. He had
started to develop an interest in natural
history some time before, while studying
medicine at Edinburgh University. The
overwhelming power of South American
biodiversity that greeted the young Charles
Darwin led him to declare that "The
elegance of the grasses, the novelty of the parasitical
plants, the beauty of the flowers, the glossy
green of the foliage, but above all the general
luxuriance of the vegetation, filled me with admiration." (Voyage of the Beagle, Chapter
I, Feb. 1832)
However, it was not only the luxuriance that influenced his mind but also the lesser plains of the south and their fossils.
Actually, he became fascinated by the discovery
of gigantic Pleistocene mammals
during his journeys in Uruguay, and the
Pampean region and Patagonian coast of
Argentina, before leaving the continent
in May 1834 (see letters sent by Charles
Darwin to Caroline Darwin and John
Stevens Henslow in Burkhardt and Smith
1985, p. 276 and 280 respectively). As
developed more fully in another contribution
(see Fernicola et al., 2009) the extraordinary
zoological collection of fossil
and extant specimens made by Charles
Darwin during his voyage to South America
was studied by an important group
of naturalists who published their conclusions
between February 1838 and October
1843 in the "The Zoology of the Voyage
of H.M.S. Beagle". All fossils mammals
included in this work were studied by
Richard Owen, who recognized the
South American ungulates Toxodon platensis
and Macrauchenia patachonica, a fossil
horse identified as Equus sp., the mastodont
Mastodon angustidens, and the ground
sloths Glossotherium sp., Mylodon darwinii,
Scelidotherium leptocephalum, Mega-lonyx jeffersonii,
Megatherium cuvierii, and the glyptodonts
Glyptodon clavipes, Hoplophorus euphractus
among xenarthrans, as well as
some smaller forms like rodents. The taxonomic
history of several of these taxa
is complex, including issues as varied as
nomenclatural problems (e.g. Megatherium
cuvierii nomen illegit.) to the mixing of
specimens of different species or genera
assigned to the same species (e.g. Megatherium
americanum), an issue that is treated
by Fernicola et al. (2009).
It is widely accepted that by the time
Darwin boarded the Beagle he had been
influenced by Lamarck's ideas on evolution
(see Woodward 1987). Also, that the
giant fossil quadrupeds he found were
significant toward the development of
his evolutionary theory, as very early they
suggested to him that the similarities between
extinct and living forms should be
explained by the existence of common
ancestors, and that the transformation of
species to a large degree was not a vertical
sequence, as Lamarck had proposed,
but a tree with asymmetric branches (see
Huxley and Kettlewell 1965). In his own
words: "to my view, in S. America parent of
all armadilloes might be brother to Megatherium
- uncle now dead" (Darwin, 1837-1838 in
Barret 1960). Woodward (1987) stated
that by that time Darwin was also familiar
with adaptation (The red notebook
of Charles Darwin in Herbert 1980, p.
67), another important biological issue
related to evolution, but an idea then
associated with Natural Theology (Paley
1802), which argued that every organism
was intentionally perfectly designed to its
particular life conditions by God.
But it was not only the idea, means and
processes of evolution that impressed
Darwin. During his journey between
Buenos Aires and Santa Fe he wrote "We
may therefore conclude that the whole area of the
Pampas is one wide sepulchre for these extinct
quadrupeds" (Voyage of the Beagle, Chapter
VII, Oct. 1833). By that time his
sharp mind had already noted "That large
animals require luxuriant vegetation has been a
general assumption, which has passed from one
work to another. I do not hesitate, however, to
say that is completely false; and that it has vitiated
the reasoning of geologists, on some points of
great interest in the ancient history of the world" (Chapter V, of the Beagle, Aug. 1833,
The red notebook of Charles Darwin in
Herbert 1980, p. 54).
In January 1834, Darwin collected remains
of Macrauchenia in Patagonia near
San Julián, in what today is Santa Cruz
province. He made inferences about the
environment in which this beast lived
and reflected on its extinction: "Mr.
Owen... considers that they form part of an animal
allied to the guanaco or llama, but fully as
large as the true camel. As all the existing members
of the family of Camelidae are inhabitants
of the most sterile countries, so we may suppose
was this extinct kind… It is impossible to reflect
without the deepest astonishment, on the changed
state of this continent. Formerly it must have
swarmed with great monsters, like the southern
parts of Africa, but now we find only the tapir,
guanaco, armadillo, capybara; mere pigmies compared
to antecedents races... Since their loss, no
very great physical changes can have taken place
in the nature of the Country. What then has exterminated so many living creatures?…We
are so profoundly ignorant concerning the physiological
relations, on which the life, and even
health (as shown by epidemics) of any existing
species depends, that we argue with still less
safety about either the life or death of any
extinct kind" (Voyage of the Beagle,
Chapter IX, Jan. 1834).
In this way, Darwin not only triggered
the studies on the genealogical interpretation
of the fossil mammal lineages, but
also opened a gate to the research on
their behaviour, physiology and extinction;
in others words, on their palaeobiology.
Phylogenetic studies, combined
with morphological and taxonomic analyses,
flourished in South America, particularly
beginning during the latter half of
the 19th century due to the intellectual
influence of Florentino Ameghino, but
palaeobiology became a much more
recent line of work, in apparent relation
to innovations in methodology and technology.
Indeed, Pleistocene South American
fossil mammals show a greater
morphological diversity than their living
counterparts, as they include representatives
of great body size and very peculiar
features. Their peculiarity and general
lack of modern analogues have encouraged
creative palaeobiological approaches
that will be outlined below.
The aim of this contribution is to overview
the recent contributions on the
palaeobiology and palaeoecology of the
Pleistocene fossil mammals of South
America, in order to investigate if we can
provide answers for the questions that
the young Darwin made himself when
he first collected them.
RECONSTRUCTING PALAEOBIOLOGY OF SOUTH AMERICAN PLEISTOCENE MAMMALS
Palaeobiologists are interested in reconstructing
the form of the fossils as living
animals, their habitat, ecological role, behaviour,
and basic biology. Vizcaíno et al. (2004) and Vizcaíno et al. (2008) describe
a basic protocol for palaeobiological studies
that identifies three biological attributes
that are essential for each taxon:
size, diet and usage of substratum or
type of locomotion. Such principles have
been used for the last three decades (e.g.,
Andrews et al. 1979, Van Couvering
1980, Reed 1998, etc.) though not fully
applied to South Aerican mammals.
Morphological study of the masticatory
and locomotor apparatuses allows predictions
on the movements for which the
apparatuses are optimized. In addition,
analyses of mastication are useful for
formulating hypotheses about the diet of
the organism, while analyses of the locomotor
apparatus allow inferences about
the type of locomotion or preferences in
the usage of substratum: runner, hopper,
digger, burrower, etc. Obviously, these
two aspects, added to body size, yield
relevant data for the interpretation of an
organism in a palaeobiological context.
Palaeomammalogists have largely applied
actualism, according to which past events
are surmised by analogy with currently
observable processes assuming that fossil
species had similar habits to their current
relatives. However, when phylogenetic
affinity is not very close or fossil lineages
possess morphologies not represented in
extant species (Vizcaíno et al. 2004), this
methodology does not provide reliable
results, a circumstance that is particularly
applicable to the mammalian faunas that
evolved in relative isolation in South
America during a good part of the Tertiary.
Vizcaíno et al. (2004) and Vizcaíno
et al. (2008) provide accounts on the reconstruction
of palaeobiology through
the application of the "form-function correlation
approach" (Radinsky 1987), according
to which function can be inferred
from form, to make good use of the
main sources of information like fossilized
bones and teeth (though indirect evidence
can also be used). Form-function
relationships can be studied through different
approaches, like functional morphology,
biomechanics and ecomorphology
(see definitions in Vizcaíno et al. 2008, and references therein)
It was not until the second part of the
1990s that authors began to apply biomechanic,
morpho-geometrical, and ecomorphological
methods to the study of
morphology as part of a major project
aimed at understanding the great palaeobiological
diversity of the South American
extinct forms. These results allowed
the development of novel interpretations
of their modes of life that, coupled with
palaeoenvironmental data (geology, palaeoclimatology
and reconstruction of
palaeovegetation), provide insightful information
on the paleoecological context
in which these animals existed.
Body size
Body size has a remarkable influence on an animal's life because it can be correlated, among other features, with metabolism, limb bone dimensions and biomechanics of locomotion, or particular solutions for food intake. Body mass in Pleistocene xenarthrans was estimated using scale and computer generated (geometric) models, and allometric equations (see Vizcaíno et al. 2008 and references therein). Using these approaches, Fariña et al. (1998), Bargo et al. (2000) and Christiansen and Fariña (2003) estimated the masses of most Lujanian megamammals. Among the late Quaternary mammals of South America, three species rival for the title of the largest of them: the giant ground sloths Megatherium americanum and Eremotherium laurillardi whose body masses must have reached between three and six tonnes, depending on the approach used (Casinos 1996, Fariña et al. 1998), and the mastodont Stegomastodon superbus, estimated at four or five tonnes. The mylodontid ground sloth Lestodon armatus (Fig. 1) follows closely, with an estimated mass of three to four tonnes, while the other my-lodontids are smaller: between one and two tonnes for Glossotherium robustum and Mylodon darwini, and with Scelidotherium leptocephalum, at 900 kg, falling just short of the megamammal category (Bargo et al. 2000). Among glyptodonts the largest was Glyptodon clavipes, individuals which may have reached nearly two tonnes. Others, though smaller, were also very large mammals: Doedicurus clavicaudatus at 1400 kg, Panochthus tuberculatus at (1100 kg), and Glyptodon reticulatus at 850 kg.
Figure 1: Life reconstruction
of Lestodon sp.
The different size of the
tusks suggest sexual
dimorphism. Drawing
by Néstor Toledo.
Scale=100 cm.
There were also non-xenarthran giants, such as the camel-like Macrauchenia and the rhinoceros-like Toxodon (Fig. 2), whose body masses must have surpassed the one tonne limit (Fariña and Álvarez 1994, Fariña et al. 2005). The Carnivora, in turn, reached impressive sizes, although well below one tonne, with the sabre-tooth Smilodon populator and the short faced bear Arctotherium spp. attaining sizes of three or four hundred kilograms (Fariña et al. 1998).
Figure 2: Life reconstruction
of Toxodon sp.
Drawing by Néstor
Toledo. Scale=100 cm.
Limbs, locomotion and habits
Biomechanical studies performed in the
last decade on large glyptodonts and
ground sloths provided insight into the
capacity of the limb bones to withstand
bending forces, forearm extension and
velocity, bipedalism or digging abilities.
Within cingulates, Fariña's (1995) analyses
of limb bones and locomotory habits
in some glyptodonts indicated that femur
strength indicators of large Pleistocene
forms were equivalent to those of large
living mammals capable of galloping (i.e.
buffalos and rhinos), but values of the
humerus were similar to those of elephants,
which cannot gallop. The muscular
insertions suggest that glyptodonts
were able to adopt bipedal postures to
perform strenuous activities, such as the
intraspecific fighting proposed by Fariña
(1995).
For the ground sloths, different specializations
may have been derived from a
primitive quadrupedal way of locomotion
in both main lineages of Pleistocene
forms, megatheriids and mylodontids.
The giant sloth Megatherium americanum has been formally proposed as bipedal
based on ichnologic and biomechanical
evidence (Aramayo and Manera de Bianco
1996, Blanco and Czerwonogora
2003). The latter includes analyses of body
size, speed, Froude number, indicator
of athletic ability, bending and resistance
moments of the vertebral column, as
well as a complete geometric and biomechanical
analysis of the footprints assigned
to this species found in Pehuén-Có,
Buenos Aires Province, Argentina. Bipedalism
also implies that the forelimb
could have been free to perform activities
other than locomotion. Fariña and
Blanco (1996) tested the possibility that
the forearms of Megatherium americanum were designed for optimizing speed
rather than strength of extension, and
concluded that such a trait may have
been associated with a potentially aggressive
use of the animal's large claws. Bargo
et al. (2000) analysed limb proportions
and resistance to bending forces in mylodontids
to infer their locomotor adaptations.
The analysis indicates that some of
them were well adapted for strenuous activities
in which force was enhanced over
velocity, such as digging. Based on this
work, Vizcaíno et al. (2001) considered
these taxa as possible builders of large
Pleistocene burrows reported in the
Pampean region (Zárate et al. 1998).
As for the strange hoofed mammals collected
by Darwin, their athleticism seems
to have been impressive in the case
of Toxodon, which must have been capable
of fast locomotion, and even more
impressive in Macrauchenia, albeit for different
reasons. Indeed, limb bone
strength of the latter was larger if measured
transversely rather than anteroposteriorly,
which has been interpreted as
the capability of suddenly turning while
being pursued by a predator (Fariña et al. 2005).
Feeding apparatus
Functional morphology and biomechanics
have been applied to the study of
feeding in a wide range of xenarthrans
(Vizcaíno et al. 2008, and references therein).
Within the Pleistocene armoured
forms, plant-eating was determined in
eutatines (Vizcaíno and Bargo 1998),
pampatheres (Vizcaíno et al. 1998, De
Iuliis et al. 2000) and glyptodonts (Fariña
and Vizcaíno 2001), although different
kinds of herbivory may have occurred in
each group. The studies also revealed
that some cingulates evolved mechanical
solutions not present in any related taxa,
and do not have current analogues that
can be used as models to investigate and
interpret adaptations of lineages without
living representatives. For instance, the
masticatory apparatus in glyptodonts underwent
a telescoping process that placed
it well below the cranium (Fariña 1985,
1988), creating problems in the way that
stresses produced by mastication were
absorbed by the mandible and implying
unusual jaw mechanics (Fariña and Vizcaíno
2001).
Bargo (2001), Bargo et al. (2006a, b), and
Bargo and Vizcaíno (2008) studied the
masticatory apparatus of the large South
American Pleistocene ground sloths. Jaw
mechanics, morphogeometric analyses,
and the correlation between cranio-dental
variables (hypsodonty, dental occlusal
surface area and relative width of the
muzzle) and diet, all suggested probable
niche differentiation among ground
sloths based on dietary categories. While
the masticatory pattern of mylodontids
is rather generalized with a clear anteromedial
powerstroke, as previously proposed
by Naples (1989), Megatherium americanum was well adapted for strong, mainly
vertical biting. This information, in addition
to tooth shape, suggests that teeth
were mainly used for cutting, rather than
grinding, and that fibrous food was not
the main dietary component.
Hypsodonty is the relative increase in
crown height of a tooth. It has been traditionally
viewed as a response to dietary shifts toward abrasive vegetation, although
recent work indicates that evolution
of hypsodonty is also due to the higher
prevalence of grit and dust in more
open environments (Bargo et al. 2006a
and references therein). Bargo et al.'s
(2006a) comparative analyses of eleven
species of Pleistocene sloths suggest that
differences in hypsodonty may be explained
by diet, habitat and behaviour.
Among mylodontids, hypsodonty was
unlikely due solely to dietary preferences,
such as grazing. As mentioned above,
some mylodontids were capable diggers
that likely dug for food, and ingestion of
abrasive soil particles probably played a
considerable role in shaping their dental
characteristics. Geographical distributions
of the megatheriids Eremotherium and Megatherium indicate differing habitats
as possible factors in hypsodonty differences.
Vizcaíno et al. (2006) investigated
the relationship between dental
occlusal surface area (OSA) and diet, and
other biological factors in fossil xenarthrans.
They found that for most fossil
xenarthrans OSA is smaller than expected
compared to 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
for by high fermentation in the digestive
tract, and/or lower metabolic requirements.
On the other hand, Megatherium
americanum has an OSA as high as, or
even higher than, that expected for a
mammal of its size, which indicates higher
oral food processing, lower fermentation
capacity, and/or higher metabolic
requirements.
Other features besides teeth are also important.
For instance, Bargo et al. (2006b)
used muzzle shape and facial musculature
reconstructions to develop models of
food intake in five species of South American
Pleistocene giant ground sloths.
Ground sloths with wide muzzles (Glossotherium
robustum and Lestodon armatus)
had a square, non-prehensile upper lip
that, coupled with the tongue, were used
to pull out grass and herbaceous plants
(mostly bulk-feeders). Sloths with narrow
muzzles (Mylodon darwini, Scelidotherium leptocephalum and Megatherium americanum)
had a cone-shaped and prehensile
upper lip (Fig. 3) that was used to select
particular plants or plant parts (mixed or
selective feeders).
Figure 3: Life reconstruction of the head of Megatherium sp. Drawing by Néstor Toledo. Scale=50 cm.
A morphofunctional approach has been less often applied to other Lujanian mammals because they are more readily comparable to living analogues. The upper incisors of Toxodon were strongly arched, whereas the lower ones were horizontally arranged. Their great lateral expansion gave the lower jaw a giant, spade-like appearance. In Macrauchenia the retracted position of the large, elliptical nostrils suggests the presence of a trunk. Considering morphological and isotopic evidence, they have been mainly considered as grazers and mixed-feeders respectively (MacFadden and Shockey 1997). Among horses, Hippidion shows a narrower nasomaxillar region, with well developed preorbital fossae and a retracted nasal notch, a combination of features that has been interpreted as an adaptation to more closed habitats, such as a savanah. Also, Hippidion shows teeth with relatively lower degree of folding in the enamel and less hypsodont than Equus (Amerhippus), which suggest a diet less rich in silica. Congruently, biogeochemical data suggest that the species of Equus (Amerhippus) had a more grazing diet than Hippidion (MacFadden et al. 1996, Mac Fadden and Shockey 1997, MacFadden et al. 1999).
PALAEOECOLOGY
As for palaeoecological interpretations,
there have been several approaches to
the study of Cenozoic South American
faunas, including feeding habits, locomotion,
and trophic relationships. Fariña
(1996) analysed the trophic relationships
of the South American Lujanian (late
Pleistocene-early Holocene) megamammals,
from the perspective of the ecological
implications of their body sizes.
Based on an estimation of population
density derived from body sizes Fariña
(1996), as Darwin realized 160 years before,
emphasized that the fauna contained
a significant diversity of large herbivores.
Conversely, according to Fariña, it
did not contain a proportionally diverse
suite of large carnivores. Assuming a basal
metabolism in agreement with the
body size of the beasts, the food energy
required to sustain the fauna was calculated.
The results suggest that based on the
requirements of the species under consideration
(i.e., mammals over 10 kg), they
alone must have needed about 1.8 megajoules
per square metre per year (hereafter,
MJ m-2 year-1) of the vegetation which
sustained them. Since a primary productivity
of 7.3 MJ m-2 year-1 is considered
excellent for modern open field ecosystems,
it is difficult to explain how the
smaller species of mammals could have
survived, let alone reptiles, birds, insects
and other consumers. If the Lujanian
plains had been as productive as the
African savannah is today, about 38 MJ
m-2 year-1, the consumption efficiency
would fall to little more than 3%, which
is a typical value for modern grassland
systems.
However, available evidence points to a
different scenario. The fossiliferous Guerrero
Member of the Luján Formation
was deposited between about 20 to 10
thousand years before present, when the
Last Glacial Maximum (LGM) was established
and, due to the extensive glaciation
in the Andes, the climate was much
dryer and decidedly cooler than present
conditions in that region (Clapperton
1983). Different sources of evidence are
congruent with this paleoclimatic interpretation
(Cantú and Becker 1988, Tonni
1990). As noted above, this was precisely
Darwin's (1839) intuition about the
landscape being less luxuriant than today.
However, it seems that it was even more
arid than surmised by the great naturalist.
Current biogeographic reconstructions for the period of the LGM show that the
Pampean plains underwent intense aeolian
activity that redeposited large masses
of silt and fine sand of periglacial origin.
Southwest from the rivers where the
sand was trapped in, a sand-sea in the
southwestern half of the Pampas was
formed, as well as a broad loessic belt
over the remainder of the area. Also, the
remains of the still-extant mammals, i.e., those whose habitat preference can be
safely assigned, belong to species confined
to Central and Patagonian faunistic
provinces (Tonni 1985, Prado et al. 1987,
Alberdi et al. 1989). The same can be said
about the birds of this age (Tonni and
Laza 1980), and analyses of pollen and
ostracods have yielded congruent results
(Quattrocchio et al. 1988, Markgraf 1989,
Prieto 1996).
According to Iriondo and García (1993),
the shift was about 750 km south west
relative to present conditions. Hence, the
place where the current city of Luján lies
would have had climatic conditions similar
to the climate that exists currently in
the northern Patagonian locality of
Choele-Choel (39ºS, Río Negro province),
whose climogram indicates a lower
mean annual temperature (2.5-3ºC less
than at the present), with more marked
seasonality (summers only about 1ºC colder
but winters up to 4ºC colder). More
importantly, the aridity must have been
higher, with rainfall considerably lower,
about 350 mm per year as compared with
the nearly 900 mm current for that area.
These figures are considered as approximations,
given the likely influence of
other factors, such as the well-known
high edaphic quality of the Pampean region,
and perhaps due to the impact of
the local water bodies, a topic discussed
below. Thus, primary productivity in the
mid-latitude Lujanian might have been
higher on average than that in today's
Choele-Choel area but it does not seem
likely that it could have been higher than
the most productive present-day cattle
field of Uruguay, and, hence, it must
have been dramatically lower than the
African savannah. As a consequence of
this reasoning, Fariña (1996) suggested
that the coexistence of so many large
herbivores in a poor environment led to
strong competition for resources. It is
worth to mention here that by the
Pleistocene large carnivorous birds, like
the phorusrhacids and theratorns had
long before become extinct in the
Pampean region. He concluded that some
of the mammals previously considered
strict herbivores might have been
flesh-eaters to some degree. After eliminating
large ungulates for varied morphological
reasons, Fariña (1996) proposed
that ground sloths were opportunistic
carrion eaters.
This challenging view, in turn, renewed
interest in other ecological topics, such as
niche partitioning in the Pleistocene and
reinterpretation of the systematics of some
South American Carnivora, among
others. For instance, Vizcaíno's (2000)
brief analysis of plant resource exploitation
among sympatric Lujanian herbivorous
armoured xenarthrans suggested
that the main dietary difference among
these cingulates was in the coarseness of
the vegetation they were capable of processing.
Bargo (2001) and Bargo et al. (2006b) proposed a niche differentiation
among Lujanian ground sloths based on
the different degrees of ability for plant
selection due to muzzle morphology.
Moreover, Vizcaíno et al. (2006) proposed
that, like living sloths (see Gilmore et
al. 2008 and references therein), mylodontids
had very low metabolism, which
suggests they were probably neither particularly
abundant nor did they require as
much food as originally calculated.
A recent revision of the bears from
South America proposed that during the
Late Pleistocene there were three species
of bears (Soibelzon 2004), instead of
one as considered by Fariña (1996). Bears
may have acted as large scavengers,
which was probably true for other carnivores
such as felids and canids as well,
forcing reexamination of Fariña's (1996)
estimates of trophic diversity, at least to a
certain extent. Prevosti and Vizcaíno
(2006) reviewed carnivore richness in the
Lujanian of the Pampean Region, describing
the palaeoecology of these species
(including their probable prey choices)
and assessing the available information
on taphonomy, carnivore ecology, and
macroecology to test the hypothesis of "imbalance" of the Río Luján fauna.
They found that the carnivore richness
of the Río Luján fauna comprises five
species: Smilodon populator, Panthera onca,
Puma concolor, Arctotherium tarijense, and Dusicyon avus, plus two other species that may be added when the Lujanian of
Buenos Aires province is included:
Arctotherium bonariense and Canis nehringi.
With the exception of D. avus and A. tarijense,
these are hypercarnivores that could
prey on large mammals (100-500 kg) and
juveniles of megamammals (>1000 kg).
Smilodon populator could also hunt larger
prey with body mass between 1000 and
2000 kg. The review of the "imbalance" hypothesis reveals contrary evidence and
allows the proposal of alternative hypotheses.
If high herbivore biomass occurred
during the Lujanian, a higher density
of carnivores could be supported.
EXTINCTION
The study of extinctions has become a
particularly relevant issue in palaeontology.
Over the last few decades, analyses
of biodiversity during the history of life
and its ups and downs, both gradual and
sudden (Sepkoski 1978, 1979, Raup and
Sepkoski 1984) have become the cornerstone
of the way we look into the
deep past. Moreover, the spectacularity
of mass extinction and of the non-actualistic
proposals of extraterrestrial causes
(Álvarez et al. 1980) attracts the attention
of academics as well as of the general
public.
The extinction of the giant mammals has
long been attributed to the purported
competition that followed the interchange
of mammalian contingents across the
Panama isthmus when it emerged some
three million years ago. Known as the
Great American Biotic Interchange, this
asymmetrically reciprocal invasion brought
carnivores (cats, dogs, mustelids, and
bears), insectivores, rodents (in addition
to the already present caviomorphs), rabbits,
mastodons, tapirs, horses, camels,
deer and peccaries to South America,
where many of those groups still thrive.
On the other hand, some South American
lineages trekked north across the
bridge: opossums, caviomorph rodents,
toxodonts, glyptodonts, armadillos (including
pampatheres), anteaters and
ground sloths, and platyrhine primates,
although not all were equally successful
or ventured equally far in their new land.
According to a proposal long held for the
first half of the 20th century (Matthew
1930, Webb 1976, Simpson 1950), the
evolutionarily advantaged northern
mammalian lineages, on their triumphal path from their alleged evolutionary cradle
in central Asia to all the corners of
the globe, outcompeted their South
American counterparts, driving them to
extinction or forcing them to take refuge
in marginal habitats. In the last part of
that century, some authors critically revised
the success of the North American
immigrants in South America (Marshall et
al. 1982, Marshall 1988, Webb 1985), and
Webb (1991) provided an ecogeographic
model that explains the assymmetrical
results of the land-mammal interchange
between both land masses. An analysis of
the pattern of Pleistocene extinction
(Lessa and Fariña 1996) revealed that
large body size, rather than continent of
origin, was the leading factor in determining
which mammals went extinct.
Another interesting issue is that of
human impact, as it relates both to the
timing of the peopling of the Americas
and to ethical, environmentally oriented
issues. Up to present, evidence of this
human impact was scarce, although some
remains do show interesting connections.
Particularly, a clavicle of a mylodontid
ground sloth found in Arroyo del Vizcaíno, Uruguay, shows marks assigned
to human activities. This specimen,
as well as others, have been dated at
about 29,000 years before present, a
much older age than the 12,000 or 13,000
ybp currently accepted for human presence
in the Americas (Arribas et al. 2001,
Fariña and Castilla 2007).
ANSWERS TO DARWIN'S QUESTIONS
As noted above, we intend here to overview
the palaeobiological and palaeoecological
contributions on the Pleistocene
mammals of South America and assess
their measure of progress in answering
young Darwin's questions and comments
on such matters. As conclusions of this
article, his assertions will be considered
one by one and our current point of view
will be added.
"We may therefore conclude that the whole area
of the Pampas is one wide sepulchre for these
extinct quadrupeds", said Darwin, and time
has corroborated this statement in its
fullest sense. Beginning with the collections
made by Francisco Muñiz and
Da´maso Larrañaga, as well as the subsequent
work of the Ameghino brothers,
the Museo de La Plata, the Museo Argentino
de Ciencias Naturales "Bernardino
Rivadavia", the Museo Nacional de
Historia Natural de Montevideo and a
multitude of smaller museums exhibit
exquisite specimens of those amazing
fossil beasts, as well as of many other remains
that are housed in collection
rooms.
"That large animals require luxuriant vegetation
has been a general assumption, which has
passed from one work to another. I do not hesitate,
however, to say that is completely false; and
that it has vitiated the reasoning of geologists, on
some points of great interest in the ancient history
of the world", claimed the young travelling
naturalist. It seems he was absolutely
right: as far as modern evidence is
concerned, climates in middle latitudes
seem to have shifted some 750 km
towards the South-West since pleniglacial
times, and hence the places where this
impressive fauna must have lived then in
a rather arid environment, as suggested
by studies on small mammals, invertebrates,
pollen and sediments, although more
precise biogeographic and ecological
hypotheses are yet in great need.
"Mr. Owen... considers that [the remains of
what today is called Macrauchenia] form part of
an animal allied to the guanaco or llama..." This statement would have been right if
referred to the fossil camelid Palaeolama.
However, Macrauchenia is not a camelid
but a Litoptern, a group not related to
any living order of mammals and its
phylogenetic relationships are yet to be
established. Nevertheless it is worth to
consider his reflection on the palaeoenvironments: "As all the existing members of the
family Camelidae are inhabitants of the most
sterile countries, so may we suppose was this
kind…It is impossible to reflect without the deepest
astonishment, on the changed state of this
continent. Formerly it must have swarmed with
great monsters, like the southern parts of
Africa, but now we find only the tapir, guanaco,
armadillo, capybara; mere pigmies compared to
antecedents races... Since their loss, no very great
physical changes can have taken place in the
nature of the Country". Darwin's astonishment
is to be shared. As is evident from
the preceding sections, not so long ago,
in geological terms, the mid latitude
plains of south eastern South America
were home to perhaps the most spectacular
mammalian fauna of all times. How
an environment of apparently such a low
productivity could support so many herbivores
remains a mystery. On the other
hand, advancements in studies in astronomical
forcing and palaeoclimatology
partially refutes Darwin's impression, as
the nature of the country has changed
since its coldest period during the LGM
(approximately 18 kybp) and sea level has
risen more than 100 m, causing vast areas
to become submerged. Ironically, the
large beasts went extinct when the climate
became less arid and the vegetation
more luxuriant. That leads us to the
following question: What then has exterminated
so many living creatures?
Extinction, a major topic in current evolutionary
thinking was surprisingly not a
major issue for Darwin. References to
the subject are scarce, although important,
in his writings and we are left to
wonder whether he accepted the ideas
common in his time of catastrophes
(Cuvier's global revolutions) having wiped
species from the Earth. On the other
hand, his proposal, many years later as a
settled gentleman living in the quiet comfort
of his Kent home, that species were
originated by means of natural selection
has been interpreted as the foundation of
modern views about extinction. In other
words, species were easily viewed as
prone to extinction if their individuals
were not fit, if their members lost in
great numbers the struggle for life. As
for the giant mammals that inspired his
thoughts as a young traveller, he was more
than eager to accept they no longer
lived, although the question why it may
have happened did not surface frequently
enough, probably accepting Cuvier's
point of view on the subject.
Our knowledge has increased considerably
since then. Today, we pay enormous
attention to this subject, due to our
growing concern about present, dwindling
biodiversity, our fascination with
the spectacular extraterrestrial causes
that have been proposed, and the ongoing
human impact on megamammals.
However, we end this article with one
last reflection.
"We are so profoundly ignorant concerning the
physiological relations, on which the life, and
even health (as shown by epidemics) of any existing
species depends, that we argue with still less
safety about either the life or death of any
extinct kind" (Voyage of the Beagle,
Chapter IX, Jan. 1834). Science has made
considerable progress since those words
were written by the person who changed
the way humankind views itself and the
rest of nature. However, we should be
persuaded that his claim, which emphasized
ignorance, be taken as a call to continue
his approach. In this context, modern
research on the marvellous beasts
that roamed South America during the
Pleistocene has indeed continued forward
on the path set out by Darwin, contributing
to the understanding of evolution
intermingled with ecology and phylogeny.
Thus, in the process of expanding
our knowledge, as often happens in
science, further ignorance has been revealed.
However, we hope that this will
only whet our appetite for the acquisition
of more knowledge.
ACKNOWLEDGEMENTS
We want to acknowledge the editors for inviting us to participate in this volume. Gerry De Iuliis read critically an early version of the manuscript. Susana Bargo, Teresa Manera, Christine Janis and Darin Croft reviewed the manuscript. Néstor Toledo made the life reconstructions.
WORKS CITED IN THE TEXT
1. Alberdi, M.T., Menegaz, J.L., Prado, J.L. and Tonni, E.P. 1989. La fauna local de Quequén Salado - Indio Rico (Pleistoceno tardío) de la provincia de Buenos Aires, Argentina. Aspectos paleoambientales y bioestratigráficos. Ameghiniana 25: 225-236.
2. Alvarez, L.W., Alvarez, W., Asaro, F. and Michel, H.V. 1980. Extraterrestrial cause for the Cretaceous-Tertiary extinction: Experimental results and theoretical interpretation. Science 208: 1095-1108.
3. Andrews, P., Lord, J.M. and Evans, E.M.N. 1979. Patterns of ecological diversity in fossil and modern mammalian faunas. Biological Journal of the Linnean Society 11: 177-205.
4. Aramayo, S.A. and Manera de Bianco, T. 1996. Edad y nuevos hallazgos de icnitas de mamíferos y aves en el yacimiento paleo iconológico de Pehuen-Co (Pleistoceno Tardío), Provincia de Buenos Aires, Argentina. Asociación Paleontológica Argentina, Publicación Especial 4: 47-57.
5. Arribas, A., Palmqvist, P., Pérez-Claros, J.A., Castilla, R., Vizcaíno, S.F. and Fariña, R.A. 2001. New evidence on the interaction between humans and megafauna in South American. Publicaciones del Seminario de Paleontología de Zaragoza 5: 228-238.
6. Bargo, M.S. 2001. The ground sloth Megatherium americanum: skull shape, bite forces, and diet. In Vizcaíno, S.F., Fariña, R.A. and Janis, C. (eds.) Biomechanics and Paleobiology of Vertebrates. Acta Paleontologica Polonica (Special Issue) 46: 41-60.
7. Bargo, M.S. and Vizcaíno, S.F. 2008. Paleobiology of Pleistocene ground sloths (Xenarthra, Tardigrada): biomechanics, morphogeometry and ecomorphology applied to the masticatory apparatus. Ameghiniana 45:175-196.
8. 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.
9. Bargo, M.S., Vizcaíno, S.F. and Kay, R.F. 2004. Evidence for Predominance of Orthal Masticatory Movements in Early Sloths. 7° International Congress of Vertebrate Morphology, Journal of Morphology 260: 276.
10. Bargo, M.S., De Iuliis, G. and Vizcaíno, S.F. 2006a. Hypsodonty in Pleistocene ground sloths. Acta Paleontologica Polonica 51: 53-61.
11. Bargo, M.S., Toledo, N. and Vizcaíno, S.F. 2006b. Muzzle of South American ground sloths (Xenarthra, Tardigrada). Journal of Morphology 267: 248-263.
12. Barret, P. 1960. Transcription of Darwin`s first notebook on "Transmutation of species". Bulletin of the Museum of Comparative Zoology at Harvard College 122(6A): 248-296.
13. Blanco, R.E. and Czerwonogora, A. 2003. The gait of Megatherium Cuvier 1796 (Mammalia, Xenarthra, Megatheriidae). Senckenbergiana Biologica 83: 61-68.
14. Burkhardt, F. and Smith, S. 1985. The Correspondence of Charles Darwin Volume 1 1821-1836. Cambridge University Press, 752 p., Cambridge.
15. Cantú, M. and Becker, A. 1988. Holoceno del arroyo Spernanzoni, Dpto. Río Cuarto, Prov. Córdoba, Argentina. International Symposium Holocene in South America, Abstracts: 24.
16. Casinos, A. 1996. Bipedalism and quadrupedalism in Megatherium: an attempt at biomechanical reconstruction. Lethaia 29: 87-96.
17. Christiansen, P. and Fariña, R.A. 2003. Mass estimation of two fossil ground sloths (Xenarthra; Mylodontidae). In Fariña, R.A., Vizcaíno, S.F. and Storch, G. (eds.) Morphological studies in fossil and extant Xenarthra (Mammalia). Senckenbergiana Biologica 83: 95-101.
18. Clapperton, C. 1993. Quaternary geology and geomorphology of South America. Elsevier, 779 p., Amsterdam.
19. Darwin, C.R. 1839. Narrative of the surveying voyages of His Majesty's Ships Adventure and Beagle between the years 1826 and 1836, describing their examination of the southern shores of South America, and the Beagle's circumnavigation of the globe. Volume III journal and remarks 1832-1836. Henry Colburn Press, 615 p., London.
20. De Iuliis, G., Bargo, M.S. and Vizcaíno, S.F. 2000.Variation in skull morphology and mastication in the fossil giant armadillos Pampatherium spp. and allied genera (Mammalia: Xenarthra: Pampatheriidae), with comments on their systematics and distribution. Journal of Vertebrate Paleontology 20: 743-754.
21. Fariña, R.A. 1985. Some functional aspects of mastication in Glyptodontidae (Mammalia). Fortschritte der Zoologie 30: 277-80.
22. Fariña, R.A. 1988. Observaciones adicionales sobre la biomecánica masticatoria en Glyptodontidae (Mammalia; Edentata). Boletín de la Sociedad Zoológica (2a. época) 4: 5-9.
23. Fariña, R.A. 1995. Limb bone strength and habits in large glyptodonts. Lethaia 28: 189-96.
24. Fariña, R.A.1996. Trophic relationships among Lujanian mammals. Evolutionary Theory 11: 125-34.
25. Fariña, R.A. and Álvarez, F. 1994. La postura de Toxodon: una nueva reconstrucción. Acta Geologica Leopoldensia 39: 565-571.
26. Fariña, R.A. and Blanco, R.E. 1996. Megatherium, the stabber. Proceedings of the Royal Society London, Series B 263: 1725-1729.
27. Fariña, R.A. and Castilla, R. 2007. Earliest evidence for human-megafauna interaction in the Americas. In Corona, M.E. and Arroyo-Cabrales, J. (eds.) Human and Faunal Relationships Reviewed: An Archaeozoological Approach, British Archaeological Reports, International Series 1627: 31-34, Oxford.
28. Fariña, R.A. and Vizcaíno, S.F. 2001. Carved Teeth And Strange Jaws: How Glyptodonts Masticated. In Vizcaíno, S.F., Fariña, R.A. and Janis, C. (eds.) Biomechanics and Paleobiology of Vertebrates. Acta Paleontologica Polonica (Special Issue) 46: 87-102.
29. Fariña, R.A., Vizcaíno, S.F. and Bargo, M.S. 1998. Body mass estimations in Lujanian (Late Pleistocene-Early Holocene of South America) mammal megafauna. Mastozoología Neotropical 5: 87-108.
30. Fariña, R.A., Blanco R.E. and Christiansen, P. 2005. Swerving as the escape strategy of Macrauchenia patachonica (Mammalia; Litopterna). Ameghiniana 42: 751-760.
31. Fernicola, J.C., Vizcaíno, S.F. and De Iuliis, G. 2009. The fossil mammals collected by Charles Darwin in South America during his travels on board the HMS Beagle. Revista de la Asociación Geológica Argentina 64(1): 147-159.
32. Gilmore, D., Fittipaldi Duarte, D. and Peres da Costa, C. 2008. The physiology of two- and three-toed sloths. In Vizcaíno, S.F. and Loughry, W.J. (eds.) The Biology of the Xenarthra, p. 130-142. University Press of Florida. Gainesville.
33. Herbert, S. 1980. The red notebook of Charles Darwin. Bulletin of the British Museum (Natural History) Historical Series 7: 1-164.
34. Huxley, J. and Kettlewell, H.B.D. 1965. Charles Darwin and his world. Viking Press, 144 p., New York.
35. Iriondo, M. and García, N.O. 1993. Climatic variations in the Argentine plains during the last 18.000 years. Palaeogeography, Palaeoclimatology, Palaeoecology 10: 209-220.
36. Lessa, E.P. and Fariña, R.A. 1996. Reassessment of extinction patterns among the late Pleistocene mammals of South America. Palaeontology 39(3): 651-662.
37. MacFadden, B.J. and Shockey, B.J. 1997. Ancient feeding ecology and niche differentiation of Pleistocene mammalian herbivores from Tarija, Bolivia: morphological and isotopic evidence. Paleobiology 23: 77-100.
38. MacFadden, B.J., Cerling, T.E. and Prado, J.L. 1996. Cenozoic Terrestrial Ecosystem in Argentina Evidence from Carbon isotopes of Fossil Mammal Teeth. Palaios 11: 319-327.
39. MacFadden, B.J., Cerling, T.E., Harris, J.M. and Prado, J.L. 1999. Ancient latitudinal gradients of C3/C4 grasses interpreted from stable isotopes of New World Pleistocene horses. Global Ecology and Biogeography 8: 137-149.
40. Markgraf, V. 1989. Palaeoclimates in Central and South America since 18,000 BP based on pollen and lake-level records. Quaternary Science Review 8: 1-24.
41. Marshall, L.G. 1988. Land Mammals and the Great American Interchange. American Scientist 76(4): 380-388.
42. Marshall, L.G., Webb, S.D., Sepkoski, J.J. Jr. and Raup, D.M. 1982. Mammalian Evolution and the Great American Interchange. Science 215(4538): 1351-1357.
43. Matthew, W.D. 1930. Range and limitations of species as seen in fossil mammal faunas. Bulletin of the Geological Society of America 41: 271-274.
44. 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.
45. Paley, W. 1802. Natural Theology. Oxford University Press, 384 p., Oxford.
46. Prado, J.L., Menegaz, A.N., Tonni, E.P. and Salamme, M.C. 1987. Los mamíferos de la fauna local Paso Otero (Pleistoceno tardío), provincia de Buenos Aires. Aspectos paleoambientales y bioestratigráficos. Ameghiniana 24: 217-233.
47. Prevosti, F. and Vizcaíno, S.F. 2006. Paleoecology of the large carnivore guild from the late Pleistocene of Argentina. Acta Palaeontologica Polonica 51: 407-422.
48. Prieto, A.R. 1996. Late Quaternary Vegetational and Climatic Changes in the Pampa Grassland of Argentina. Quaternary Research 45: 73-88.
49. Raup, D.M. and Sepkoski, J.J. Jr. 1984. Periodicity of extinctions in the geologic past. Proceedings National Academy of Sciences 81: 801-805.
50. Quattrocchio, M., Deschamps, C., Martínez, D., Grill, S. and Zavala, C. 1988. Caracterización paleontológica y paleoambiental de sedimentos cuaternarios, Arroyo Napostá Grande, Provincia de Buenos Aires. 2º Jornadas Geológicas Bonaerenses, Actas: 37-46, Buenos Aires.
51. Radinsky, L.B. 1987. The Evolution of Vertebrate Design. The University of Chicago Press, 188 p., Chicago.
52. Reed, K.E. 1998. Using large mammal communities to examine ecological and taxonomic structure and predict vegetation in extant and extinct assemblages. Paleobiology 24: 384-408.
53. Sepkoski, J.J. Jr. 1978. Kinematic model of Phanerozoic taxonomic diversity 1: analysis of marine orders. Paleobiology 4: 223-251.
54. Sepkoski, J.J. Jr. 1979. Kinematic model of Phanerozoic taxonomic diversity 2: early Phanerozoic families and multiple equilibria. Paleobiology 5: 222-251.
55. Simpson, G.G. 1950. History of the fauna of Latin America. American Journal of Science 38: 361-389.
56. Soibelzon, L. 2004. Revisión sistemática de los Tremarctinae (Carnivora, Ursidae) fósiles de América del Sur. Revista del Museo Argentino de Ciencias Naturales "Bernardino Rivadavia" 6: 107-133.
57. Tonni, E.P. 1985. Mamíferos del Holoceno del Partido de Lobería, Provincia de Buenos Aires. Aspectos paleoambientales y bioestratigráficos del Holoceno del sector oriental de Tandilia y Área Interserrana. Ameghiniana 22: 283-288.
58. Tonni, E.P. 1990. Mamíferos del Holoceno en la Provincia de Buenos Aires. Paula-Coutiana 4: 3-21.
59. Tonni, E.P. and Laza, J.H. 1980. Las aves de la Fauna local Paso de Otero (Pleistoceno tardío) de la provincia de Buenos Aires. Su significación ecológica, climática y zoogeográfica. Ameghiniana 17: 313-322.
60. Van Couvering, J.A.H. 1980. Community evolution in Africa during the Cenozoic. In Berensmeyer, A.K. and Hill, A. (eds.) Fossils in the Making, University of Chicago Press, p. 272-298, Chicago.
61. 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.
62. Vizcaíno, S.F. and Bargo, M.S. 1998. The masticatory apparatus of Eutatus (Mammalia, Cingulata) and some allied genera. Evolution and paleobiology. Paleobiology 24: 371-383.
63. Vizcaíno, S.F., Zárate, M., Bargo, M.S. and Dondas, A. 2001. Pleistocene burrows in the Mar del Plata area (Buenos Aires Province, Argentina) and their probable builders. In Vizcaíno, S.F., Fariña, R.A. and Janis, C. (eds.) Biomechanics and Paleobiology of Vertebrates. Acta Paleontologica Polonica, Special Issue 46(2): 157-169.
64. Vizcaíno, S.F., De Iuliis, G. and Bargo, M.S. 1998. Skull shape, masticatory apparatus, and diet of Vassallia and Holmesina (Mammalia: Xenarthra: Pampatheriidae). When anatomy constrains destiny. Journal of Mammalian Evolution 5: 293-321.
65. Vizcaíno, S.F., Fariña, R.A., Bargo, M.S. and De Iuliis, G. 2004. Phylogenetical assessment of the masticatory adaptations in Cingulata (Mammalia, Xenarthra). Ameghiniana 41: 651-664.
66. Vizcaíno, S.F., Bargo, M.S. and Cassini, G.H. 2006. Dental occlusal surface area in relation to food habits and other biologic features in fossil Xenarthrans. Ameghiniana 43: 11-26.
67. Vizcaíno, S.F., Bargo, M.S. and Fariña, R.A. 2008. Form, Function and Paleobiology in Xenarthrans. In Vizcaíno, S.F. and Loughry, W.J. (eds.) The Biology of the Xenarthra, University Press of Florida, p. 86-99, Gainesville.
68. Webb, S.D. 1976. Mammalian faunal dynamics of the Great American interchange. Paleobiology 2: 216-234.
69. Webb, S.D. 1985. Late Cenozoic mammal dispersal between the Americas. In Stehli, F.G. and Webb, S.D. (eds.) The Great American Biotic Interchange, Plenum Press, p. 201-217, New York.
70. Webb, S.D. 1991. Ecogeography and the great American interchange. Paleobiology 17(3): 266-280.
71. Woodward, J. 1987. Darwin. Editorial Alianza, 141 p., Madrid.
72. Zárate, M.A., Bargo, M.S., Vizcaíno, S.F., Dondas, A. and Scaglia, O. 1998. Estructuras biogénicas en el Cenozoico tardío de Mar del Plata (Argentina) atribuibles a grandes mamíferos. Revista de la Asociación Argentina de Sedimentología 5: 95-103.
Recibido: 5 de agosto de 2008
Aceptado: 5 de octubre de 2008