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Old World Ruminant Morphophysiology, Life History, and Fossil Record: Exploring Key Innovations of a Diversification Sequence

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The omasum of pecoran ruminants (which is absent in tragulids) and shorter gestation periods in non-giraffid crown pecorans (as opposed to giraffids) could represent cases of key innovations that caused disparity in species diversity in extant ruminants. Literature suggests that the different ruminant groups inhabited similar niche spectra at different times, supporting the ‘increased fitness’ interpretation where a key innovation does not mainly open new niches, but allows more efficient use of existing ones. In this respect, we explored data on fossil species diversity of Afro-Eurasian ruminants from the Neogene and Quaternary. Tragulid and giraffid diversity first increased during the Early/Middle Miocene with subsequent declines, whereas bovid and cervid diversity increased distinctively. Our resulting narrative, combining digestive physiology, life history and the fossil record, thus provides an explanation for the sequence of diversity patterns in Old-World ruminants.
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Ann. Zool. Fennici 51: 80–94 ISSN 0003-455X (print), ISSN 1797-2450 (online)
Helsinki 7 April 2014 © Finnish Zoological and Botanical Publishing Board 2014
Old world ruminant morphophysiology, life history, and
fossil record: exploring key innovations of a diversication
sequence
Marcus Clauss1,* & Gertrud E. Rössner2,3,4
1) Clinic of Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich,
Winterthurerstr. 260, CH-8057 Zurich, Switzerland (*corresponding author’s e-mail: mclauss@
vetclinics.uzh.ch)
2) SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Str. 10,
D-80339 Munich, Germany
3) Department für Geo- und Umweltwissenschaften, Ludwig-Maximilians-Universität München,
Richard-Wagner-Strasse 10, D-80333 München, Germany
4) GeoBio-Center LMU, Richard-Wagner-Strasse 10, D-80333 München, Germany
Received 3 Apr. 2013, nal version received 4 Sep. 2013, accepted 4 Sep. 2013
Clauss, M. & Rössner, G. E. 2014: Old world ruminant morphophysiology, life history, and fossil
record: exploring key innovations of a diversication sequence. — Ann. Zool. Fennici 51: 80–94.
The omasum of pecoran ruminants (which is absent in tragulids) and shorter gesta-
tion periods in non-girafd crown pecorans (as opposed to girafds) could represent
cases of key innovations that caused disparity in species diversity in extant ruminants.
Literature suggests that the different ruminant groups inhabited similar niche spectra
at different times, supporting the ‘increased tness’ interpretation where a key innova-
tion does not mainly open new niches, but allows more efcient use of existing ones.
In this respect, we explored data on fossil species diversity of Afro-Eurasian ruminants
from the Neogene and Quaternary. Tragulid and girafd diversity rst increased during
the Early/Middle Miocene with subsequent declines, whereas bovid and cervid diver-
sity increased distinctively. Our resulting narrative, combining digestive physiology,
life history and the fossil record, thus provides an explanation for the sequence of
diversity patterns in Old-World ruminants.
Introduction
Evolutionary progress and key
innovations
That progress occurred during evolutionary his-
tory at a macroevolutionary level is usually not
an issue of debate (e.g. Rosenzweig & McCord
1991). From the anatomy of the rst multicel-
lular organisms to complex plants and animals,
from the structure of the rst terrestrial tetra-
pod’s limb to the unguligrade extremity of larger
herbivores (Shubin et al. 2006, O’Leary et al.
2013), from the addition of the hypocone to the
molar morphology of therian mammals (Hunter
& Jernvall 1995) — the concept of progress in
functional morphology appears intuitive. What
is often debated is progress at a microevolution-
ary level: why does a certain taxonomic group
appear to be more successful in terms of spe-
ANN. ZOOL. FENNICI Vol. 51 Tragulid and pecoran diversity 81
ciation than another, like certain spider clades
(Bond & Opell 1998) or a certain clade among
phyllostomid bats (Dumont et al. 2012)? Can
we explain this in terms of evolutionary progress
and a hypothetical, more efcient functionality,
maybe even linked to a certain (and potentially
new) niche, in the sense of ‘directional evolu-
tion’ (Liem 1990), or do we choose to consider
morphophysiological variety at low taxonomic
levels as random variety solving the same prob-
lems in different ways (of similar efciency) in
the sense of neutral evolution (ibid.)?
The concept of key innovation plays an
important role in the more general concept of
evolutionary progress; key innovations may
explain competitive displacement (Nitecki 1990,
Rosenzweig & McCord 1991, Heard & Hauser
1995, Hunter 1998). Morphophysiological,
behavioural and life history peculiarities of a
certain clade do not only help to dene that clade
taxonomically, but represent potential candidates
for innovations that helped shape that clade’s
evolutionary success. However, apart from rare
exceptions when fossils also reveal details, e.g.
of copulation (Joyce et al. 2012), pregnancy,
precociality and birth (Gingerich et al. 2009), or
sociality (Bibi et al. 2012), mostly only a certain
subset of morphological attributes fossilizes. The
emphasis in the concept of key innovations has
therefore traditionally been on hard tissue mor-
phological aspects (Burggren & Bemis 1990).
One perceived problem with the concept of
key innovation is the tautology amounting from
the likewise usage of morphological characters
to identify a (diverse) clade and as a reason
for its success (diversity). The recent develop-
ment of deriving phylogenetic estimates from
genetic information alleviates this problem and
facilitates statistical approaches to test for the
effect of certain morphological characteristics
on diversication rates in extant species clusters
(e.g. Dumont et al. 2012). For most fossil taxa,
however, the lack of genetic material means that
the problem is not readily alleviated. Another
solution is to use a character considered to be
apomorphic or convergent in several different
taxa, which can be compared to closely related
taxa in which it is absent (e.g. Hunter & Jernvall
1995). Thus, studies of key innovations in the
fossil record often represent narratives, in which
the plausibility of the argument is the major indi-
cator of its quality, but the underlying hypothesis
cannot be tested statistically.
Hence, phenotypic traits without a potential
to fossilize such as soft tissue anatomy, physiol-
ogy and life history characteristics provide ideal
bases to explore key innovations, because they
are usually not used to reconstruct phylogenetic
relationships. Under the assumption that those
traits observed in extant species are representa-
tive for the entire clade including fossil spe-
cies, the adaptive value of such features can be
assessed in comparative and even experimental
studies on extant species. A prominent example
where soft tissue anatomy and physiology was
used to explain the evolutionary diversication
is the digestive physiology of ungulate her-
bivores. Using the concept of a difference in
the digestive function of hindgut and foregut
fermenters (Janis 1976, Duncan et al. 1990),
Janis et al. (1994) have explained the apparent
displacement of equids by ruminants, conclud-
ing a primarily digestion-driven evolutionary
advantage for ruminants. Similarly, the differ-
ence in species diversity between Tylopoda and
Ruminantia was speculated to result from the
differences in functionality of the sorting mecha-
nism that prevents Tylopoda from achieving the
higher food intakes observed in many Ruminan-
tia (Clauss et al. 2010a). This latter hypothesis
correlates well with the apparent replacement
of camelids by ruminants in Janis et al. (1994).
Because of their prominence in specimen and
species number in the fossil record, and detailed
knowledge about their comparative anatomy and
physiology (Clauss et al. 2008), ungulate her-
bivores appear as promising test cases for the
exploration of evolutionary success and related
key innovations.
Tragulidae, Pecora, and ruminant
stomach anatomy
Compelling evidence of extended comparative
analyses including phenotypic as well as molec-
ular data (Janis & Scott 1987, Gentry & Hooker
1988, Hernández-Fernández & Vrba 2005, Has-
sanin et al. 2012) supports the view that Traguli-
dae are the sister group of Pecora, and the most
82 Clauss & Rössner ANN. ZOOL. FENNICI Vol. 51
basal living ruminant group. The branch-off of
the tragulid clade from the ruminant stem lin-
eage is biostratigraphically/biochronologically
dated for the Late Eocene in southeast Asia
(Métais et al. 2001). Molecular clock analyses
produced contradicting estimates for the Late
Eocene (Hernández-Fernández & Vrba 2005)
or Late Oligocene to Early Miocene (Hassanin
et al. 2012). The pecoran branch-off has been
estimated via molecular clock analyses at 33.2 to
27.6 million years ago (mya) (Early Oligocene to
Late Oligocene) (Hernández-Fernández & Vrba
2005, Hassanin et al. 2012).
The ten currently differentiated species of
Tragulidae (Groves & Grubb 2011) stand in
contrast to the overall pecoran species number of
200 to more than 300 (dependent on species con-
cepts used). Moreover, the very differently sized
Pecora (body masses from 2 kg in Madoqua to
1500 kg in Giraffa) inhabit nearly all terrestrial
habitats from coast to high mountains and from
equator to subpolar regions (Wilson & Mitter-
meier 2011), whereas all of the tragulids are of
small size, and inhabit exclusively dense forest
undergrowth or thickets within these forests
in Africa and southeast Asia (Meijaard 2011).
Although very few peer-reviewed reports on
their natural diet exist (but see Dubost 1984),
extant tragulids are commonly considered to be
selective feeders with a major component of fruit
and additional browse (Meijaard 2011). This is
supported by a correlation of tragulid density
with the abundance of fruit (Heydon & Bolloh
1997). In contrast, the fossil record of tragulids
points to a diverse evolutionary history with a
substantial diversication at the beginning of the
Miocene or even end of the Oligocene (Geraads
2010, Sánchez et al. 2010). It documents a wide
geographical distribution covering vast parts of
Afro-Eurasia, large ranges of body sizes (more
than twice the size of the largest extant species),
skeletodental morphologies, preferred diets, and
habitats as well as a common sympatric occur-
rence of up to four species in the Miocene
(23.03 to 5.3 mya) (Mottl 1961, Fahlbusch 1985,
Pickford 2001, Rössner 2004, 2007, Barry et
al. 2005, Eronen & Rössner 2007, Kaiser &
Rössner 2007, Ungar et al. 2012). In particular,
dietary reconstructions for fossil tragulids indi-
cate a spectrum that ranges from fruit-dominated
to pure browse diets and mixed diets with a dis-
tinctive monocot component (Kaiser & Rössner
2007, Ungar et al. 2012); tragulids have there-
fore recently been considered ‘ecological precur-
sors’ of bovid ruminants (Ungar et al. 2012).
The ruminant digestive system is character-
ised by a multi-compartmental forestomach that
harbours a physiological sorting mechanism, fol-
lowed by a glandular stomach that is the homo-
logue of the simple stomach of other mammals
(Clauss & Hofmann 2014). The morphology of
the ruminant forestomach varies between rumi-
nant species in many characteristics (Hofmann
1973, 1989, Clauss et al. 2006, 2009a, 2010b,
Clauss & Hofmann 2014), but there is one
major difference between the two infraorders
of ruminants, the Pecora (in the modern world
represented by families Bovidae, Moschidae,
Cervidae, Girafdae, Antilocapridae) and the
paraphyletic “Tragulina” (in the modern world
represented only by Tragulidae) (Fig. 1). The
Fig. 1. Schematic representation of the stomach of
tragulids (top) and Pecora (bottom). Rum = rumen, Ret
= reticulum, Om = omasum (lacking in tragulids), Abom
= abomasum. Drawing by Jeanne Peter, after Schmidt
(1911) and Hofmann (1969).
ANN. ZOOL. FENNICI Vol. 51 Tragulid and pecoran diversity 83
pecoran stomach represents the ruminant condi-
tion as known from domestic species: four func-
tionally different compartments, comprising the
rumen (the major site of microbial fermentation),
the reticulum (the site of the sorting mechanism),
the omasum (the site of re-absorption of uid
that is used for both the sorting mechanism
and harvest of microbes from the rumen), and
the abomasum (the glandular stomach) (Clauss
& Hofmann 2014). In contrast, the stomach of
tragulids only comprises three compartments —
it is lacking the omasum (Milne-Edwards 1864,
Schmidt 1911, Vidyadaran et al. 1982). The
absence of the omasum in tragulids has been
considered one of many anatomical traits that
reect either a basal phylogenetic position of
tragulids among extant ruminants (Langer 1988)
or a highly derived position with secondarily
achieved primitive traits among pecorans (Boas
1890). The latter assumption has not found sup-
port in subsequent studies on ruminant phy-
logeny. The ruminant sorting mechanism in the
reticulum depends on a high moisture content
in this organ. Digesta with such a high moisture
content is highly diluted. If such digesta would
pass on into the abomasum, the abomasum
would have to secrete high amounts of acid and
gastric enzymes to compensate for that dilution.
The addition of an omasum between the reticu-
lum and the abomasum could therefore represent
an advantage as it re-absorbs signicant amounts
of the moisture from the digesta.
Girafdae, crown Pecora, and ruminant
gestation periods
Opinions on the phylogenetic position of Giraf-
dae within crown Pecora have changed con-
stantly before times of molecular/morphomo-
lecular analyses (e.g. Gentry 1994, 2000, Has-
sanin & Douzery 2003). Meanwhile, there is
broad consensus on the origin of Girafdae
laying within crown Pecora prior to all other
included clades except Antilocapridae (e.g. Janis
& Scott 1987, Hernández-Fernández & Vrba
2005, Hassanin et al. 2012). According to the
fossil record (Harris et al. 2010), the African
origin of girafds (Gentry 2000) dates back
at least to 19 mya (Solounias 2007). Giraffoid
ancestors of girafds could have originated from
Eurasian stem pecorans (Gelocidae) before the
Early Miocene. Coincidentally, molecular clock
analyses produced dates of origin for girafds in
the Late Oligocene (Hassanin & Douzery 2003,
Hassanin et al. 2012).
The nine currently differentiated species
of Girafdae (Brown et al. 2007, Groves &
Grubb 2011) also stand in contrast to the overall
number of crown pecoran species. The giraffe
(Giraffa spp.), usually considered the largest
extant ruminant (Clauss et al. 2003) with a body
mass of up to 1500 kg, has a widespread distri-
bution across subsaharan Africa savannas, and
the unique feeding adaptation of a long neck that
ensures a feeding niche not attained by any other
ruminant (Cameron & du Toit 2007). In contrast,
the okapi (Okapia johnstoni), with a body mass
in the range of antelope at 250 kg, has a very
limited distribution range in the Itulu forest of
Zaire (Skinner & Mitchell 2011). Both genera
are considered very strict browsers that nearly
always avoid the intake of grass forage (Skinner
& Mitchell 2011); both genera are also prime
examples of brachydont ruminants (Janis 1988).
Similarly as with the fossil record of tragulids,
the fossil record of girafds indicates a diverse
evolutionary history with a substantial diver-
sication during the Middle and Late Miocene
(Gentry & Heizmann 1996, Harris et al. 2010),
including a wide geographical distribution range
in the Old World, a variety of skeletodental
morphologies, preferred diets, and habitats as
well as a common sympatric occurrence of up
to four species in the Late Miocene (Gentry &
Heizmann 1996, Harris et al. 2010). Although
a characteristic feature of girafds is the always
comparably large body size among contempora-
neous ruminants, there was, and still is between
Giraffa and Okapia, a considerable body size
diversity in this group (Solounias 2007). In par-
ticular, dietary reconstructions for fossil girafds
indicate a spectrum that covers the whole range
from browsing to grazing (Solounias et al. 2000,
2010, Cerling et al. 2005).
Among the ruminants, girafds are peculiar
because of evident differences in life history:
both the maximum longevity and the gestation
time are distinctively longer in girafds (Müller
et al. 2011a, Clauss et al. 2014) (Fig. 2). Reasons
84 Clauss & Rössner ANN. ZOOL. FENNICI Vol. 51
why girafd newborns, which are of a similar
degree of precociality as bovid or cervid new-
borns, require these dramatically longer gesta-
tion times for their development are, to our
knowledge, unknown. Because short gestation
times will reduce generation intervals, and may
represent an important adaptation to seasonal
environments (Zerbe et al. 2012), this differ-
ence could put girafds at a disadvantage, both
in terms of geographical range they can exploit
competitively, and in niche competition with
crown Pecora of shorter generation intervals.
Aim of this study
With this study, we aim at documenting the
taxonomic distribution pattern of Old World-
ruminants known so far through the Younger
Cenozoic. Given the reasons to suspect a more
efcient function of the forestomach in Pecora
(with an omasum) than in tragulids (without
an omasum), we expect that Pecora replaced
tragulids during the course of evolutionary his-
tory. Hence, the ruminant fossil record should
show a gradual shift of the taxonomic composi-
tion from a predominance of tragulids towards
a clear dominance of pecoran families. Given
the reasons to suspect a more efcient mode
of reproduction in non-girafd crown Pecora,
we expect that these groups replaced girafds
during evolutionary history. Again, the fossil
record should document a decline in the propor-
tion of girafd species with a parallel increase of
the proportion of non-girafd crown Pecora.
Material and methods
In order to provide a comparative frame for the
analysis of pecoran/tragulid faunal composition
over time, we compiled a data matrix of docu-
mented fossil ruminant species. Since tragulid
origins are still debated (see above), we focused
on reliably taxonomically allocated tragulids
from the Afro-Eurasian Cenozoic and spatiotem-
porally coinciding Pecora.
The number of Old World ruminant species
was compiled from the Miocene to the Holocene
(exclusive Recent) by generation of species
occurrences from the NOW database (Fortelius
2012). The master data matrix was downloaded
on 23 May 2012. A split of this matrix into
taxonomic data subsets follows basically the
classication into families; some uncertain taxo-
nomic cases were categorized as Pecora indet.
The geographic regions Eurasia and Africa were
treated individually. In doing so, the Arabian
Peninsula was considered a part of Africa for the
Miocene and a part of Eurasia in time intervals
younger than the Miocene according to Popov
et al. (2004). The master matrix and all the data
subsets are available from the authors on request.
Absolute numbers of species were counted
for the shortest time intervals possible to be dif-
ferentiated when correlating the different age
0
50
100
150
200
250
300
350
400
450
500
1 10 100
1000
Gestation length (days)
Body mass (kg)
Tragulidae
Giraffidae
other Pecora
Fig. 2. Gestation peri-
ods in extant ruminants
(cf. Müller et al. 2011a).
Note the distinctively
longer gestation periods
in the two extant girafds
(Okapia johnstoni, Giraffa
camelopardalis) as com-
pared with other rumi-
nants.
ANN. ZOOL. FENNICI Vol. 51 Tragulid and pecoran diversity 85
concepts used in NOW. Correlations of dif-
ferent age concepts were made using the lit-
erature (Qiu et al. 1999, Popov et al. 2004,
Hilgen et al. 2012). Taxonomic data subsets
were separated for time intervals Early Miocene
(23.03 to 15.97 mya), Middle Miocene (15.97
to 11.63 mya), Late Miocene (11.63 to 5.33
mya), Pliocene (5.33 to 2.59 mya), Pleistocene
(2.59 to 0.0117 mya), and Holocene (0.0117 to
before Recent). In addition, we separated Euro-
pean Land Mammal Zones of the Neogene (MN
zones) and correlates in Asia and Africa within
the Early Miocene to obtain a higher resolution
for the Early Miocene (because of the low spe-
cies number in MN1 and MN2 (see Fig. 3), data
were only evaluated from MN3 (~19.75 to ~18.0
mya) (Hilgen et al. 2012) and MN4 (~18.0 to
~16.9 mya) (Hilgen et al. 2012). We did not dis-
tinguish between earliest MN5 (Early Miocene)
and the rest of MN5 (Middle Miocene) (Hilgen
et al. 2012), but included all MN5 species in
the Middle Miocene. Species with imprecise
age indications were excluded from our analysis
(e.g. “Miocene” or “MN4/MN6”).
Species counts do not include taxa listed
as “indet.” or “sp.” unless there is just a single
one for the respective interval, in which case it
was counted as the only species. Species listed
as “indet.” or “sp.” were counted only when no
other species of the same genus was listed for
the same time interval. Genera listed as “indet.”
were counted only when no other genus was
listed for the same time interval. “sp.” was
always preferred against “indet.”. In the analysis
we used the superordinate taxa Giraffoidea, Cer-
voidea (excluding Andegamerycidae and Palae-
omerycidae) and Bovoidea as count categories
in order to include several species which have
only been identied more similar to one pecoran
family than to another. Apart from some excep-
tions, we did not modify the taxonomic content
of the data subsets. Exceptions are taxa listed
in NOW as Giraffoidea (Walangania, “Gelo-
cus whitworthi, Propalaeoryx, Prolibytherium,
Sperrgebietomeryx, Orangemeryx, Namibiome-
ryx, Canthumeryx), which have been revised as
Pecora indet. (Gentry 1994, Cote 2010), and taxa
listed in NOW as Moschidae (Amphitragulus,
Dremotherium, Pomelomeryx, Friburgomeryx),
which were excluded (Sánchez et al. 2010)
and compiled as Pecora indet. here. Listings of
tragulid Dorcatherium naui older than European
Land Mammal Unit MN9 were considered D.
crassum with the exception of Przeworno 1 and
2 (Czyżewska & Stefaniak 1994, see Alba et
al. 2011). Late Middle Miocene Dorcatherium
naui records from Abocador de Can Mata, Spain
(Alba et al. 2011) and Gratkorn, Austria (Gross
et al. 2011) are not yet included in NOW, but
were taken into account. D. rogeri was con-
sidered constantly a synonym of D. vindebo-
nense (Thenius 1952), as well as D. libiensis a
synonym of D. pigotti (Geraads 2010). Further,
we included additional information on occur-
0
50
100
150
200
250
300
350
MN1 MN2 MN3 MN4 Middle
Miocene
Late
Miocene
Pliocene Quaternary
Number of species
Africa
Eurasia
Fig. 3. Number of ruminant species recorded in different time intervals in Africa and Eurasia. For a denition of
MN1–MN4, see Material and methods.
86 Clauss & Rössner ANN. ZOOL. FENNICI Vol. 51
rence and age of African tragulids from Pickford
(2001), Geraads (2010), and Ungar et al. (2012).
Results
In general, the database inquiry provides species
counts, which document a constantly increas-
ing number of ruminants both in Africa and
Eurasia during the Younger Cenozoic, with a
peaking pattern of different magnitude in the
two continents (Fig. 3), reecting results from
earlier studies (e.g. Gentry 1994, 2000, 2010a,
2010b, Gentry & Heizmann 1996, Gentry et
al. 1999, Barry et al. 2005, Costeur & Legen-
dre 2008, Bibi et al. 2009, Cote 2010, Geraads
2010, Harris et al. 2010, Bibi 2011). However,
disparity in species numbers of the different
ruminant groups is evident for all time spans dif-
ferentiated. Whereas Bovoidea, Giraffoidea, and
Cervoidea in general always dominated rumi-
nant faunas [with the exception of tragulid pre-
dominance of African MN3 (Fig. 4a)], species of
unknown pecoran allocation and extinct pecoran
families (Andegamerycidae, Palaeomerycidae)
decreased over time (missing species portion
plus insignicant number of Moschidae repre-
sent difference to 100% in Fig. 4). Tragulidae
represented substantial portions of the overall
ruminant fauna in the Early/Middle Miocene (in
accord with Pickford 2001, Eronen & Rössner
2007), but do not show such a signicant spe-
cies number predominance in the Early Miocene
of Eurasia (Fig. 4b) as documented from Africa
(Fig. 4a). In Africa (Fig. 4a), Bovoidea, and
in Eurasia (Fig. 4b), Bovoidea and Cervoidea
became dominant from the Middle Miocene
onward, and Tragulidae decreased at the same
time to very few species. The Giraffoidea had a
general species diversity peak in the Middle/Late
Miocene, but never reached Bovoidea or Cervoi-
dea in species number and decreased in propor-
tion afterwards (Fig. 4) as shown and discussed
by Gentry and Heizmann (1996), Gentry (2000)
and Costeur and Legendre (2008).
Discussion
Diversication sequence
The result of the database inquiry clearly dis-
plays the remarkable Early Miocene Old World
radiation of crown Pecora, the different species
diversity peaks and spatiotemporal abundance of
Tragulidae, Cervoidea, Bovoidea, and Giraffoi-
dea, as well as their predominance and replace-
ments through the Cenozoic. With the excep-
tion of Bovoidea and Cervoidea in the Eurasian
Pliocene and Quarternary, there is no evidence
for a diversity balance between the different
ruminant groups.
Indeed, the sequence of diversity peaks and
the overall pattern reect the nearly complete
replacement of tragulids by Pecora within the
Early and Middle Miocene, and of girafds
by cervids and bovids in the Pliocene, leaving
just a handful of records for both groups in the
0
20
40
60
80
100 ab
MN3 MN4 Middle
Miocene
Late
Miocene
Pliocene Quaternary
Species (% all species)
Tragulidae Giraffoidea Bovoidea
0
20
40
60
80
100
MN3 MN4 Middle
Miocene
Late
Miocene
Pliocene
Quaternary
Tragulidae Giraffoidea Cervoidea Bovoidea
Fig. 4. Proportion (%) of species numbers of different ruminant groups recorded from different subsequent periods
in (a) Africa and (b) Eurasia. The difference to 100% represents pecoran species with unknown higher taxonomical
afliation, species from extinct pecoran families, and insignicant Moschidae. See Material and methods for details.
ANN. ZOOL. FENNICI Vol. 51 Tragulid and pecoran diversity 87
Holocene. This disparity necessarily implies a
narrowing of the habitat range, which is sup-
ported by palaeodiet reconstructions for fossil
tragulids, which cluster with living browsers and
mixed feeders in contrast to frugivorous habits
of living tragulids (Kaiser & Rössner 2007,
Ungar et al. 2012), and by paleodiet reconstruc-
tions of fossil girafds, which cover the whole
browser to grazer spectrum, in contrast to the
strict browse diet of extant species (Solounias et
al. 2000, 2010, Cerling et al. 2005). In contrast
to our expectations, only records from Africa
produce a clear pattern of succession in terms of
species majority, but not those from Eurasia. In
Eurasia, the Pecora, and on a lower taxonomic
level the bovids and cervids, always represented
the highest proportion of species at any time
investigated in this study. The major difference
in the diversication sequences of Africa and
Eurasia is the always signicant proportion of
cervids in Eurasia. If cervids remain uncon-
sidered, a more or less similar diversication
sequence is evident for Africa and Eurasia. With
respect to the question of key innovations we
wanted to answer, it appears as if the ‘superior-
ity’ of the Pecora already shaped species diver-
sity in Eurasia from the Early Miocene onwards
as also described by Gentry (1994, 2000) —
essentially driven by early cervid diversica-
tion. Morphophysiological differences especially
between cervids and bovids, and potential expla-
nations for their difference in modern ecological
and geographical distribution ranges, are dis-
cussed elsewhere (Heywood 2010).
Explanations as narratives
An important limitation of this study is that
no real test of the relevance of the omasum
can be performed, due to the absence of other
ungulate groups in which the course of species
diversity over time in clades with a forestomach
with and without an omasum-like structure can
be compared. In extant organisms, a statistical
evaluation of diversication rate and charac-
ters considered key innovations is possible (e.g.
Bond & Opell 1998, Dumont et al. 2012); in the
fossil record, such an evaluation is feasible if the
character in question evolved in several differ-
ent clades, such as the hypocone in mammalian
molars (Hunter & Jernvall 1995). In the absence
of such conditions, the major qualitative test of
the hypothesis put forward is the plausibility of
the argument (Jensen 1990, Rohde 1996). For
this, the observation that clades without the key
innovation covered a similar niche range, at
least in terms of reconstructed diets, is impor-
tant. Similar broad diet ranges mean that differ-
ences in diversication patterns cannot be easily
explained by shifts in the proportion of habitats
or resources available to ruminants, but must
be sought in other factors (such as the proposed
key innovations). Yet, the problem remains in
accounting for the higher diversity of one group
with a key innovation. One never knows if this
one detail was really the key to success, or if
there was a multitude of other factors. Ulti-
mately, explanations for species diversity pat-
terns as presented here must be considered (plau-
sible) narratives (Carcraft 1990). With respect to
the life history parameter used in our explanation
(gestation period length), differences in other
mammal groups, though beyond the scope of
this study, could be used to test for a similarity
in diversication sequence, with more recently
radiated taxa having shorter gestation periods.
The ruminant forestomach
The major peculiarity of the ruminant forestom-
ach is its sorting mechanism. It ensures that only
small particles are passed out of the reticulum,
whereas larger ones are retained. This depends
on a density gradient of particles on the one hand
(Baumont & Deswysen 1991, Lechner-Doll et
al. 1991), and on the presence of a uid environ-
ment in the reticulum on the other, in which den-
sity-based sorting by otation and sedimentation
can occur. Therefore, the reticulum contents are
always particularly moist in ruminants (Clauss et
al. 2009b, 2009c). When digesta is passed from
the reticulum to the lower digestive tract, this
digesta therefore will contain a high moisture
content, which constitutes a dilution factor that
will require a high secretion output in the subse-
quent stomach and intestinal regions. One of the
major functions of the omasum as it is understood
today is the absorption of uid from the digesta
88 Clauss & Rössner ANN. ZOOL. FENNICI Vol. 51
that leave the reticulum (reviewed in Clauss et
al. 2006). Correspondingly, the digesta in the
omasum are invariably much drier than in the
reticulum (Clauss et al. 2009b, 2009c) and also
than in the subsequent glandular stomach, where
acid and enzyme secretions increase the moisture
content again. Notably, this uid-reabsorption
function should not be linked to a putative adap-
tation to dry environments; actually, those rumi-
nant species with the largest omasum (cattle rela-
tives; Clauss et al. 2006) are the ones that have
the highest uid loss in their faeces and thus def-
ecate in ‘pies’ (Clauss et al. 2003, 2004). Rather
than relating to the uid homeostasis of the whole
organism, the omasum is associated with the uid
regulation within the stomach complex. The addi-
tion of the omasum between the reticulum and
the abomasum could therefore help reducing the
workload on the secretory cells and thus represent
an energy and protein saving mechanism.
Additionally, the omasum might allow rumi-
nants to evolve a high-uid throughput strategy
through the reticulorumen that is a characteristic
of the so-called ‘cattle-type’ ruminants (Clauss
et al. 2010a). The additional benet of this high
uid throughput was rst suspected to lie in the
formation of a ‘bre raft’, and the associated
increased efciency of the sorting mechanisms
and a ‘lter bed-effect’ that delays the excretion
of small particles and thus facilitates an even
more efcient digestion (Clauss et al. 2008).
However, it could be shown that the efciency
of the sorting mechanism does not differ in a
relevant way between ‘moose-type’ ruminants
with a low, and ‘cattle-type’ ruminants with a
high, uid throughput (Lechner et al. 2010).
Correspondingly, tragulids, whose uid pas-
sage pattern in the forestomach matches that of
‘moose-type’ ruminants (Darlis et al. 2012), do
not stand out among ruminants in terms of faecal
particle size reduction (Clauss et al. 2002). But,
the important additional advantage of a high
uid throughput through the forestomach could
lie in the additional harvest of microbes that
are washed out at a high rate (Hummel et al.
2008, Clauss et al. 2010a, Müller et al. 2011b).
Thus, more microbes reach the abomasum and
small intestine per unit time, where they are
digested. By the higher harvest rates, the rumi-
nal microbe pool is manipulated towards higher
growth rates, and is therefore utilized more ef-
ciently. Such a strategy may only be feasible if
an omasum prevents the negative dilution effects
of a high forestomach uid throughput. Notably,
a ‘moose-type’ strategy does not prevent animals
from ingesting grass or mixed grass/browse diets
in an experimental setting (Lechner et al. 2010)
or when no other competitors are present. For
example, the reindeer is an outlier to a general
pattern, because its natural diet includes much
more grass than one would expect based on its
‘moose-type’ rumen physiology (the major out-
lier in the dataset of Codron & Clauss 2010); this
species hardly faces competition from sympatric
grazers. In most real ecological settings, ‘moose-
type’ ruminants are limited to browse-dominated
diets, whereas ‘cattle-type’ ruminants dominate
grass or mixed grass/browse diet niches (Codron
& Clauss 2010). This difference matches the
observed reduction of the tragulid niche to that
of ‘moose-type’ ruminants.
Gestation period
Gestation period is an important life history
measure that contributes to the overall reproduc-
tion potential of a species. Shorter gestation peri-
ods are commonly linked to shorter generation
intervals, or to a higher maximum population
growth rate, and gestation period can therefore
serve, to a limited extent, to characterise spe-
cies’ life history on a ‘slow-fast continuum’
(Bielby et al. 2007). In general, given ecological
similarity between species under no particular
resource constraint, one would expect a faster-
reproducing species to ‘outcompete’ a slower
one. Additionally, the length of the gestation
period is relevant for reproduction in seasonal
environments, as it will determine if species can
reproduce in synchrony with seasonal varia-
tion without losing reproductive potential (Kiltie
1988, Owen-Smith 1988). Modications of ges-
tation period might therefore be part of a set of
adaptations that facilitates the invasion of new,
more seasonal, environmental niches (Zerbe et
al. 2012). Although the length of the gestation
period can vary intraspecically with a variety of
factors (reviewed in Clements et al. 2011), gesta-
tion period is a reliable species-specic measure
ANN. ZOOL. FENNICI Vol. 51 Tragulid and pecoran diversity 89
that allows inter-specic comparisons (Ogutu et
al. 2010, Clements et al. 2011).
The long gestation periods observed in
girafds exceed one year. This makes girafds
the only pecoran group that is unable to adopt a
seasonal breeding pattern (that would be advan-
tageous in more temperate climates) without
losing breeding potential due to longer periods
of reproductive inactivity (Zerbe et al. 2012).
The fact that girafd diversity was proportion-
ally lower in Eurasia, with a putatively more
temperate climate, than in Africa (e.g. Bruch
et al. 2007), supports the interpretation that
they might be less successful in seasonal envi-
ronments (Fig. 4). The suggested advantage of
shorter gestation periods in bovids and cervids
does not only apply to the comparison of these
clades to girafds, but also to perissodactyls,
especially equids (Grange & Duncan 2006), and
camelids (Clauss et al. 2014). This life history
characteristic might therefore have played an
additional role — apart from the differences in
digestive morphophysiology mentioned in the
Introduction — in large mammalian herbivore
species diversication patterns. As mentioned
above, it would be interesting to check whether
more recently diversied taxonomic groups of
other clades also have comparatively shorter
gestation periods. Notably, the morphophysi-
ological mechanisms behind such life history
differences remain to be identied.
‘Increased tness’ key innovations
The key innovations mentioned in this study
belong to the group of ‘increased tness’ key
innovations sensu Heard and Hauser (1995); such
innovations do not open a particular new niche or
lead to increased specialisation (as would ‘new
adaptive zone’ or ‘specialisation’ innovations),
but increase the general efciency of organismal
function. A typical feature of such innovations is
that the clade that diversied (due to that inno-
vation) does not necessarily occupy a new or
specialised niche but covers a similar broad niche
spectrum as its predecessors, or an even broader
one. Examples for such innovations are the mam-
malian molar hypocone (Hunter & Jernvall 1995),
ungulate hypsodonty (Feranec 2007), the evolu-
tion of a ‘cattle-type’ rumen physiology with a
high uid throughput through the rumen (Codron
& Clauss 2010), and maybe also short gestation
periods (Clauss et al. 2014). One characteristic of
these increased tness key innovations yet to be
proven is that they are not costly during ontogeny
or life. This would limit them to specic environ-
mental conditions. Another characteristic of such
‘increased tness’ key innovations scenarios is
that apparent ‘specialists’ remain of the preceding
pre-innovation clades, such as the brachydont,
omasum-free tragulids, or the brachydont, long
gestation period girafds, or ‘moose-type’ rumi-
nants with a low uid throughput through the
rumen in general. The parsimonious interpretation
is that these specialists inhabit niches in which the
key innovation cannot take effect, either because
it does not offer a selective advantage in that
peculiar niche, or because this niche requires par-
ticular adaptations that cannot be reconciled with
the key innovation (McNabb 2012). In the case of
the remaining, small-bodied tragulids, the puta-
tive disadvantage of a lacking omasum may not
come into play in the strictly frugivorous/brows-
ing niche, because ruminants in that niche depend
on saliva rich in tannin-binding proteins. The
production of such saliva possibly precludes the
production of the high saliva volumes necessary
for a high uid throughput strategy (Hofmann
et al. 2008, Clauss et al. 2010a, 2011, Codron
& Clauss 2010). Without an omasum, tragulids
could thus survive in diet niches otherwise occu-
pied by ‘moose-type’ ruminants such as duikers
(Clauss et al. 2011). Extant girafds survive in
their unique feeding niches, either because of their
long neck and associated morphophysiological
adaptations that are unique in ruminants (Cam-
eron & du Toit 2007, Mitchell & Skinner 2010)
in the case of the giraffe, or because of historical
contingency in the Itulu forest in the case of the
okapi. Identifying the conditions that allow those
species not endowed with a key innovation to per-
sist in their niches is an important part of explain-
ing the relevance of key innovations.
Conclusion
To conclude, this study provides a plausible
but not exhaustive narrative that explains the
90 Clauss & Rössner ANN. ZOOL. FENNICI Vol. 51
sequence of diversication and evolutionary dis-
parity patterns in ruminants from the beginning
of the Neogene to Extant, with an emphasis on
innovative characters of digestive morphophysi-
ology and life history. A similar ruminant specic
diversication sequence can be derived from the
data collection in Jardine et al. (2012) for a
longer time span in North America, with a peak
of traguloid species diversity in the Eocene and
a subsequent decline and concomitant increasing
diversity of Pecora from the Oligocene onward.
Obviously, it would be interesting to compare
ruminant diversity patterns in earlier time peri-
ods in the Old World.
Whereas the tragulid forestomach anatomy
may have conserved an earlier developmental
stage of the digestive tract in ruminant evolution,
the pecoran forestomach added the omasum.
This difference in the overall efciency of the
forestomach may have made tragulids suscep-
tible to resource competition in the context of
increased openness of landscapes during the
Neogene, and their fall a contemporaneous event
to the initial major diversication of pecorans.
The omasum, a hallmark of the pecorans, and
especially developed in the most recently radi-
ated bovids, may well be the decisive innova-
tion that sets the ruminant digestive strategy
apart from that of other herbivores. Tragulids
only survived in forested relic areas in which a
frugivorous diet is possible year-round. Here, the
pecoran’s advantage will not be as pronounced
as on grass or browse-dominated diets. Thus,
today’s frugivorous adaptation of tragulids does
not necessarily represent an ancestral (living
fossil) state of this clade, an often-stated view
(e.g. Janis 1984, Thenius 2000), but rather a
secondary restriction (in correspondence with
Ungar et al. 2012).
For reasons unknown, extant girafds have
particularly long gestation periods compared to
other ruminants. Whether this life history param-
eter is the proxy for a basic physiological differ-
ence remains unknown to date. Girafds survive
only either in a peculiar geographic niche [that
may well represent a secondary niche into which
the species had to retreat (Thenius 1992)] in the
case of the okapi, or a peculiar feeding adapta-
tion (Cameron & du Toit 2007) in the case of the
giraffe.
The example of the differently speciose
groups in different geographical regions —
bovids only in Africa, and bovids and cervids
in Eurasia — indicate that apart from processes
linked to key innovations, biogeographical dis-
tribution also needs to be included in the expla-
nation of species diversication patterns. The
cause of the obviously signicant ecological role
of cervids in Eurasia, which had an immense
impact on tragulid and girafd radiation, is
unknown yet.
Acknowledgements
We thank Daryl Codron for checking the language of this
manuscript, and reviewers Suvi Viranta (Helsinki) and Zhang
Zhaoqun (Beijing) for their comments and suggestions. This
contribution is dedicated to Mikael Fortelius, whose work
and personality have inspired many researchers in paleontol-
ogy and biology. While death is ultimately always inevitable,
with Mikael, glory is, too.
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This article is also available at http://www.annzool.net/
... This was true also for their Miocene ancestors, although those were common all over Africa and in wide areas in Asia and Europe (e.g. Arambourg 1933;Whitworth 1958;Geraads 2010;Clauss and Rössner 2014). The African fossil record of tragulids suggests a first appearance of the clade in the Early Miocene (Arambourg 1933;Whitworth 1958;Pickford 2001Pickford , 2002Geraads 2010). ...
... In this context see also Lange-Badré and Böhme (2005) for Oligocene European creodonts. Rössner (2004), Clauss and Rössner (2014), and Guzmán-Sandoval (2018) compiled data proving the ecological dominance of tragulids among Ruminantia in the Early Miocene and in the Middle Miocene proportional occurrence decrease among Ruminantia contemporaneously to their diversity peak in the Middle Miocene. ...
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Tragulids are ruminant artiodactyls living today in two distinct areas in Central Africa (Hyemoschus) and South plus South east Asia (Moschiola, Tragulus). Their fossil record, however, is distributed much more widely including Europe. Yet, their palaeobiogeography and phylogeography is not fully understood. Taxonomy in need of revision, limited data and biochronological controversies hamper the reconstruction of the irevolutionary history. This study provides a taxonomic revision of tragulid faunas from late Early Miocene to early Middle Miocene sites at Napak (Uganda), which include the oldest known record on the African continent. Morphological and metrical characters of dentition supports the presence of ? Siamotragulus songhorensis in Iriri Member (ca. 20.5 Ma), Napak Member (ca. 20.5–19 Ma), and Akisim Member (ca.16 Ma). ?Siamotragulus aff. songhorensis, ?Siamotragulus n. sp., and ?Afrotragulus sp. are documented sporadically in the Iriri and Napak Member. Dorcabune iririensis and Dorcabune chappuisi as well as Dorcatherium pigotti and Dorcatherium n. sp. are recorded in the Napak Member . The results confirm the previously described successive appearance with ?S. songhorensis followed by Dorcatherium (now Dorcatherium and Dorcabune). However, our data suggest a higher diversity than previously thought, and accordingly we provide a partially alternative interpretation of the evolutionary history of Miocene African tragulids.
... Les valeurs les plus négatives sont retrouvées chez les tragulidés, chez les spécimens appartenant au genre Dorcatherium (δ 18 ODorcatherium = 23,7‰). Ce groupe est particulièrement inféodé aux environnements forestiers ou galeries forestières, proches de points d'eau, utiles pour certaines espèces actuelles pour la fuite lors d'attaques prédatrices (Clauss et Rössner, 2014 ;Rössner et Heissig, 2013 Ségalen, 2003et White, 1986. ...
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Depuis des années, les rongeurs sont étudiés pour la diversité de leurs adaptations locomotrices. Cette dernière est représentée dans le registre fossile des gisements du Miocène inférieur de Napak (Karamoja, Ouganda) et de Grillental, Elisabethfeld et Langental (Sperrgebiet, Namibie). Plusieurs espèces ont été étudiées : Paranomalurus bishopi, Paranomalurus walkeri, Nonanomalurus soniae, Renefossor songhorensis (Napak), Bathyergoides neotertiarius (Namibie) et Diamantomys luederitzi (représentée dans les deux régions). Après avoir actualisé leur systématique, les analyses morphométriques ont permis la prédiction de leur locomotion via leur crâne, humérus, ulna et fémur. Ces adaptations sont liées à la stabilisation et mobilité des membres, les arboricoles privilégiant une mobilité plus accrue, tandis que les terrestres et fouisseurs favorisent la stabilisation. Ainsi, les espèces du genre Paranomalurus sont prédites comme planeuses, N. soniae arboricole, et B. neotertiarius fouisseuse. D. luederitzi est considérée comme une espèce généraliste. La variabilité de ces comportements souligne une hétérogénéité des environnements Miocène, démontrée par les analyses isotopiques des δ13C et δ18O des carbonates de leur émail dentaire. En effet, l’analyse indique un milieu ouvert à plantes C3 dominantes avec la présence d’îlots boisés (savane arborée), confirmé par les locomotions de ces espèces. Ces rapports isotopiques couplés avec ceux des grands mammifères indiquent un environnement plus humide et/ou à température moins élevée qu’aujourd’hui dans ces localités, la région namibienne étant moins humide et potentiellement plus chaude que l’Afrique de l’Est à cette époque.
... This has already been supposed based on molecular data 28 . The rapid morphological diversification at the base of these pecoran clades may represent the effect of an ecological opportunity 30 since only these pecoran clades entered Africa at this precise period, while few other ruminants are known prior to that time from Africa [31][32][33] . Other more significant evolutionary accelerations occur at terminal nodes in clades with recent radiative events (Supplementary Data 1). ...
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Extrinsic and intrinsic factors impact diversity. On deep-time scales, the extrinsic impact of climate and geology are crucial, but poorly understood. Here, we use the inner ear morphology of ruminant artiodactyls to test for a deep-time correlation between a low adaptive anatomical structure and both extrinsic and intrinsic variables. We apply geometric morphometric analyses in a phylogenetic frame to X-ray computed tomographic data from 191 ruminant species. Contrasting results across ruminant clades show that neutral evolutionary processes over time may strongly influence the evolution of inner ear morphology. Extant, ecologically diversified clades increase their evolutionary rate with decreasing Cenozoic global temperatures. Evolutionary rate peaks with the colonization of new continents. Simultaneously, ecologically restricted clades show declining or unchanged rates. These results suggest that both climate and paleogeography produced heterogeneous environments, which likely facilitated Cervidae and Bovidae diversification and exemplifies the effect of extrinsic and intrinsic factors on evolution in ruminants.
... The causes of such a dramatic depletion of the Giraffidae is yet poorly understood. Clauss and Rössner (2014) assumed that the extremely long gestation period (more than one year) could be one of possible causes of South Asian giraffids decline, since this physiological constraint impeded giraffids to adapt to seasonal environmental conditions. The decline of late Miocene giraffids in Southern Asia coincided with the evolutionary radiation of plesiometacarpal cervids (subfamily Cervinae) in Southeast Asia. ...
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... The giraffoid clade now consists only of Giraffes, Okapis and Pronghorns [5] but they were much more widespread in the Miocene era [6]. They are now restricted to a few species in marked comparison with the enormous expansion of the other ruminant clades, in particular the Bovidae. ...
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Introduction: Mature granulated trophoblast binucleate cells (BNC) have been found in all ruminant placentas examined histologically so far. BNC are normally fairly evenly distributed throughout the fetal villus and all their granules contain a similar variety of hormones and pregnancy associated glycoproteins (PAGs). Only the Giraffe is reported to show a different BNC protein expression, this paper is designed to investigate that. Results: Gold labelled Lectin histochemistry and protein immunocytochemistry were used on deplasticised 1 μm sections of a wide variety of ruminant placentomes with a wide range of antibodies and lectins. Results: In the Giraffe placentomes, even though the lectin histochemistry shows an even distribution of BNC throughout the trophoblast of the placental villi, the protein expression in the BNC granules is limited to the BNC either in the apex or the base of the villi. Placental lactogens and Prolactin (PRL) are present only in basally situated BNC: PAGs only in the apical BNC. PRL is only found in the Giraffe BNC which react with many fewer of the wide range of antibodies used here to investigate the uniformity of protein expression in ruminant BNC. Discussion: The possible relevance of these differences to ruminant function and evolution is considered to provide a further example of the versatility of the BNC system.
... O sistema enzimático da digestão dos ruminantes depende de microrganismos que fazem a digestão de fibras vegetais. Estes localizam-se no rúmen (câmara fermentativa), onde os carboidratos estruturais dos vegetais são desdobrados em ácidos graxos voláteis (AGV's) úteis ao metabolismo do animal (Berchielli et al., 2011;Clauss & Rössner, 2014). Os AGV's produzidos pela ação fermentativa são ácido acético, o ácido propiônico e o ácido butírico que são absorvidos nos pró-ventrículos, sendo eles a principal fonte de energia para os ruminantes. ...
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A indigestão vagal é definida como uma patologia gastrointestinal não infecciosas dos ruminantes, caracterizada por distúrbios que acometem o nervo vago, e causam alterações motoras nos pré-estômagos desses animais. A indigestão vagal se baseia em quatros tipos: O tipo I acontece pela falha do esvaziamento ruminal por disfunção cárdica, o tipo II por uma estenose funcional anterior com hipermobilidade, o tipo III ocorre em função da estenose funcional posterior, enquanto que o tipo IV é identificada como indigestão de gestação tardia. Para o diagnóstico necessita-se de exames clínicos associado a laboratoriais por se tratar de sinais clínicos inespecíficos que variam de acordo com o local de comprometimento do nervo vago. O paciente diagnosticado com indigestão vagal apresenta prognóstico desfavorável. O tratamento consiste em sessões terapêuticas, administração de bicarbonato, fistulação e/ou canulação do rúmen, e até mesmo, por causa da etiologia multifatorial da indigestão vagal, procedimentos cirúrgicos. Conclui-se, então, que, a indigestão vagal é uma síndrome de grande importância na medicina veterinária, que acomete e causa desordens no trato digestório dos bovinos, e estudar sobre essa enfermidade se faz necessário para garantir e tornar mais amplo o conhecimento de doenças que acometem os ruminantes.
... One suggestion is that a longer gestation period put them at a disadvantage compared to bovids, which could better adapt to climate change by adopting seasonal breeding patterns (Clauss and Roessner, 2014). This might also explain why giraffids were never numerous in the Eurasian fauna (Fig. 1b), where they faced additional competition from deer and their kin (Cervidae). ...
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