ORIGINAL PAPER
A New Pliocene Capybara (Rodentia, Caviidae) from Northern
South America (Guajira, Colombia), and its Implications
for the Great American Biotic Interchange
María E. Pérez1,2 & María C. Vallejo-Pareja3,4 & Juan D. Carrillo5 & Carlos Jaramillo3
# Springer Science+Business Media New York 2016
Abstract One of the most striking components of the modern
assemblage of South American mammals is the semiaquatic
capybara (Caviidae, Hydrochoerinae), the biggest rodent in the
world. The large hydrochoerines are recorded from the middle
Miocene to the present, mainly in high latitudes of South
America. Although less known, they are also recorded in low
latitudes of South America, and in Central and North America.
We report the first record of capybaras from the late Pliocene of
Colombia, found in deposits of the Ware Formation, Guajira
Peninsula in northeastern Colombia. We analyze the phyloge-
netic position within Caviidae, the possible environmental
changes in the Guajira Peninsula, and the implications of this
finding for the understanding of the Great American Biotic
Interchange. The morphological and phylogenetic analyses in-
dicate that the hydrochoerine of the Guajira Peninsula is a new
species, ?Hydrochoeropsis wayuu, and this genus is most close-
ly related to Phugatherium. According to the latest phylogenetic
results, this clade is the sister group of the lineage of the recent
capybaras (Neochoerus and Hydrochoerus). ?Hydrochoeropsis
wayuu is the northernmost South American Pliocene
hydrochoerine record and the nearest to the Panamanian bridge.
The presence of this hydrochoerine, together with the fluvio-
deltaic environment of theWare Formation, suggests that during
the late Pliocene, the environment that dominated the Guajira
Peninsula was more humid and with permanent water bodies, in
contrast with its modern desert habitats.
Keywords Caviomorphs . Hydrochoerinae . Neogene .
Neotropics . Phylogeny . GABI
Introduction
The mammal assemblage that inhabits the Neotropics today
(Neotropical region sensu lato; Morrone 2014) comprises about
30 % of the extant mammalian species of the world (Wilson and
Reeder 2005; Patton 2015) including groups such as rodents
(caviomorphs and sigmodontines), primates (platyrrhine mon-
keys), bats (e.g., phyllostomids), marsupials (e.g., opossums),
and xenarthrans (armadillos, sloths, and anteaters) (Patterson
and Costa 2012). This exceptional diversity of mammals and
the multiple endemisms are the result of long periods of isolation
of South America duringmost of the Cenozoic (Wilf et al. 2013),
and the heterogeneity of the landscape and environments (e.g.,
tropical rain and dry forests, montane forests, highland grass-
lands, shrublands, savannas, and deserts; Solari et al. 2012) that
Electronic supplementary material The online version of this article
(doi:10.1007/s10914-016-9356-7) contains supplementary material,
which is available to authorized users.
* María E. Pérez
mperez@mef.org.ar
María C. Vallejo-Pareja
vacama@gmail.com
Juan D. Carrillo
juan.carrillo@pim.uzh.ch
Carlos Jaramillo
JaramilloC@si.edu
1 CONICET,Museo Paleontológico Egidio Feruglio, Av. Fontana 140,
U9100GYO Trelew, Chubut, Argentina
2 Researcher Associate FieldMuseum of Natural History, Chicago, IL,
USA
3 Smithsonian Tropical Research Institute, P.O. Box 0843-03092,
Panama City, Republic of Panama
4 Department of Biological Sciences, Sam Houston State University,
Huntsville, TX, USA
5 Paläontologisches Institut und Museum, University of Zurich,
Zurich, Switzerland
J Mammal Evol
DOI 10.1007/s10914-016-9356-7
characterize the Neotropical Region. This habitat heterogeneity is
the outcome of sea transgressions, tectonic events with the subse-
quent elevation of the Andes, global climate change, and the rise
of the Panamanian land bridge (Garzoine et al. 2008;Woodburne
2010; Farris et al. 2011; Bacon et al. 2015; Montes et al. 2015).
With the completion of the Isthmus of Panama and the
development of environments favorable to migration, the iso-
lation of South America ended, leading to the main phases of
the Great American Biotic Interchange, or GABI (Woodburne
2010; Bacon et al. 2015, 2016; Carrillo et al. 2015). During
this process many mammals native to South America, includ-
ing marsupials, xenarthrans, platyrrhine monkeys, chirop-
terans, and caviomorph rodents (porcupines, hutias, agoutis,
pacas, capybaras, spiny rats), crossed to Central and North
America (Webb 2006). Among the caviomorph lineages, por-
cupines and capybaras were the ones that reached the farthest
north (Simpson 1928; Mones 1991; Morgan 2005; Morgan
and Emslie 2010; Vucetich et al. 2015b).
Within the caviomorph rodents, one of the most striking
groups is the capybaras (Hydrochoerinae) because of their large
body size, gregarious social behavior, adaptation to a semiaquat-
ic mode of life (Mares and Ojeda 1982; Woods 1984; Eisenberg
and Redford 2000; Rowe and Honeycutt 2002; Ojasti 2011;
Oliver and Sachser 2011; Moreira et al. 2013; García-Esponda
and Candela 2016), and their ever-growing cheek teeth with
derived and complex morphology (Vucetich et al. 2005, 2012,
2014, 2015a, b). The extant large hydrochoerines are represented
by two gigantic semiaquatic species: Hydrochoerus
hydrochaeris, distributed from Argentina to Colombia, and
H. isthmius, in northwestern Colombia and Panama (Wilson
and Reeder 2005). In contrast, their fossil record indicates that
they were more diverse than today. The fossil record of
hydrochoerines is abundant, particularly for the late Miocene
of temperate South America. Fossil hydrochoerines include bas-
al forms traditionally named as Bcardiomyines^ (middle
Miocene – Pliocene) and a more derived clade, the capybaras,
that includes numerous species of Cardiatherium,
Hydrochoerus, Neochoerus, and the largest hydrochoerines,
Phugatherium and Hydrochoeropsis (Vucetich et al. 2005,
2014, 2015b; Deschamps et al. 2007, 2009, 2013; Vucetich
and Pérez 2011; Pérez et al. 2014). The hydrochoerines are
recorded from the middleMiocene to the present, mainly in high
latitudes of South America (from Argentina including northern
Patagonia, Uruguay, Chile, Bolivia; see Deschamps et al. 2013).
Although less well known, they have also been recorded in low
latitudes of South America (Urumaco and San Gregorio forma-
tions, Venezuela, Vucetich et al. 2010; Acre Region, Peru and
Brazil, Frailey 1986; Sant’anna-Filho 1994; Pleistocene deposits
of Soata, Colombia, Villarroel et al. 1996, 2001), the Caribbean
(Grenada, Lesser Antilles,MacPhee et al. 2000), andCentral and
North America (Carranza-Castañeda and Miller 1988; Mones
1991; Morgan 2005).
The capybaras only occur near permanent water bodies
such as marshes, estuaries, and along rivers and streams.
Although both extant species of Hydrochoerus currently in-
habit most of Colombia (Aldana-Dominguez et al. 2013), they
are absent in the Guajira Peninsula of northeastern Colombia
(Fig. 1), a region characterized by dry, open areas (Haffer
1967). Here, we report the first record of capybaras
(Rodentia, Caviidae) from the late Pliocene of Colombia,
found in deposits of the Ware Formation on the Guajira
Peninsula (Moreno et al. 2015); we analyze the possible en-
vironmental changes in the Guajira Peninsula during this time,
along with the implications of this discovery for our under-
standing of the Great American Biotic Interchange.
Geological Settings The recently described Ware Formation
(Moreno et al. 2015) is an important geological unit of the
Cocinetas Basin that crops out in the Department of Guajira,
northeast Colombia (Fig. 1). The Ware Formation is dominat-
ed by detrital deposits of fluvial-deltaic origin with high fossil
content. According to macroinvertebrate biostratigraphy and
isotope chronostratigraphy, it is late Pliocene in age
(Piacenzian stage ca. 3.6 to 2.5 Ma; Hendy et al. 2015;
Fig. 1 Location and stratigraphic provenance of ?Hydrochoeropsis
wayuu, new species. On left, map of South America, Colombia (inset)
and the Guajira Peninsula, indicating the place where the fossil was
found. Shaded area points out the limit between Colombia and
Venezuela. Scale bar equals 1 km. On right, stratigraphic column of
Estación de Policia Section, Ware Formation. Black bone shows the strat-
igraphic provenience of ?Hydrochoeropsis wayuu
J Mammal Evol
Moreno et al. 2015). The Ware Formation is correlated chro-
nologically with the San Gregorio Formation in the Falcon
Basin of Venezuela (Moreno et al. 2015). The vertebrate as-
semblage of the Ware Formation includes sharks and rays
(Carcharhiniformes, Myliobatiformes, and Rajiformes); three
orders of bony fish (Characiformes, Perciformes, and
Siluriformes); reptiles, represented by Crocodilia and
Testudines; and seven mammalian orders (Artiodactyla,
Carnivora, Cingulata, Litopterna, Notoungulata, Pilosa, and
Rodentia) (Forasiepi et al. 2014; Moreno et al. 2015;
Moreno-Bernal et al. 2016; Amson et al. in press). The base
of the Ware Formation, where the assemblage of mammals is
recorded, was deposited in a fluvio-deltaic environment
(Hendy et al. 2015; Moreno et al. 2015).
Materials and Methods
Institutional abbreviations. — FMNH, Field Museum of
Natural History, Chicago. MUN, Mapuka Museum,
Universidad del Norte, Barranquilla, Colombia. STRI,
Smithsonian Tropical Research Institute, Panama.
Dental nomenclature. — Tooth terminology follows
Vucetich et al. (2005) and is explained in Fig. 2.
Dental abbreviations. — c3, third internal column; h.1i.,
internal fifth fissure; h.2i., internal second fissure; h.3i., internal
third fissure; h.5i., internal fifth fissure; h.f.e., external funda-
mental fissure; h.s.e., external secondary fissure;H.F.I., internal
fundamental fissure; H.P.E., external primary fissure; H.S.E.,
external secondary fissure; h.sn.i, supernumerary internal flexid;
M1, first uppermolar;M2, second uppermolar;M3, third upper
molar; p4, fourth lower premolar; P4, fourth upper premolar;
pr.I/Pr.I, prism I; pr.II/Pr.II, prism II; pr.s.a., anterior second-
ary prism.
Morphological Description Description includes compari-
sons with other hydrochoerine species. Dental and skull mea-
surements are in Tables 1 and 2.
Phylogenetic Analysis In order to test the phylogenetic posi-
tion of the hydrochoerine of the Guajira Peninsula within
Caviidae, we performed a cladistic analysis using the com-
bined matrix of Madozzo-Jaén and Pérez (2016). Although
Kerodon is the living sister group to Hydrochoerus, it was
omitted from this analysis because it is the most basal lineage
within Hydrochoerinae and beyond the scope of our study.
The combined matrix (Online Resource 1) consists of 55 taxa
of Cavioidea, 117 morphological characters (Online Resource
2), and 4014 characters from DNA sequences (12 s, cytb,
TTH, GHR) obtained from GenBank. Some multistate char-
acters of the morphological partition were considered as addi-
tive based on increasing degrees of similarity between the
character states or in cases of interested homologies. This
dataset was analyzed using equally weighted parsimony in
TNT 1.1 (Goloboff et al. 2008a, b), and gaps were treated as
missing data for DNA sequences. We used equally weighted
parsimony to minimize the number of postulated evolutionary
transformations. The heuristic search consisted of 1000
replicates of Wagner trees with random addition se-
quence of taxa, followed by TBR branch swapping, col-
lapsing zero-length branches under the strictest criterion.
After this procedure, a final round of TBR branch
swapping was applied to find all most parsimonious
trees (MPTs). Support values were calculated using
Bremer indices, Bootstrap, and Jacking techniques.
Unstable taxa in the set of MPTs were identified using
IterPCR (Pol and Escapa 2009) to derive an informative
reduced consensus.
Fig. 2 Dental nomenclature in lower and upper teeth. aM1 or M2 (first
or second upper molar); b M3 (third upper molar); c p4 (lower fourth
premolar). Abbreviations: C3, third internal column; e.f., external
fissures; h.1i., internal fifth fissure; h.2i., internal second fissure; h.3i.,
internal third fissure; h.5i., internal fifth fissure; h.f.e., external
fundamental fissure; h.s.e., external secondary fissure; H.F.I., internal
fundamental fissure; H.P.E., external primary fissure; H.S.E., external
secondary fissure; pr.I/Pr.I, prism I; pr.II/Pr.II, prism II; pr.s.a.,
anterior secondary prism
J Mammal Evol
Distribution Analysis For analysis of the paleobiogeographic
distribution, we used all occurrences of all Hydrochoerinae in
the Paleobiology Database (PDBD; Alroy 2013), including
numerous records of our own that we added to the
PBDB. The data were downloaded from the PBDB on
April 23, 2015, using the following parameters: taxa to
inc l ude = Cav i idae and Hydrochoe r i dae , t ime
intervals = Neogene and Quaternary, region = North
America and South America, include occurrences generically
indeterminate = yes. All records of species and genus
within Hydrochoerinae were grouped into five clades,
Caviodon, Cardiatherum, Hydrochoerus + Neochoerus,
Hydrochoeropsis, and Phugatherium. The occurrences
of every clade were mapped into four intervals, 10–
5.3 Ma (late Miocene), 5.3 to 2.7 Ma (Pliocene), 2.7
to 0.01 Ma (Pleistocene), and younger than 10,000 years
(Holocene). Within the Hydrochoeropsis clade, 14 occur-
rences were excluded from the analysis for being erroneous
synonyms of species of the genus Luantus (L. toldensis,
L. propheticus, and L. minor; belonging to the basal forms
of Caviidae) with the genus Hydrochoeropsis (see Online
Resource 4).
Body Size Estimate To estimate the body size of
?Hydrochoeropsis wayuu we measured the femur length and
diameter and used the allometric equations for rodents pre-
sented by Millien and Bovy (Millien and Bovy 2010).
Results
Systematic Paleontology
Rodentia Bowdich, 1821
Hystricognathi Tullberg, 1899
Cavioidea (Fisher von Waldheim, 1817) Kraglievich 1930
Caviidae Fisher von Waldheim, 1817
Hydrochoerinae (Gray, 1825) Gill 1872:Weber 1928 sensu
Kraglievich 1930
Hydrochoeropsis Kraglievich, 1930
Type species. — Hydrochoeropsis dasseni Kraglievich,
1930
Referred species. —?Hydrochoeropsis wayuu
Table 1 Dental measurements of ?Hydrochoeropsis wayuu, new
species (in millimeters). AP, antero-posterior length AW, anterior width;
HFI, Fundamental internal flexus;HPE, primary external flexus;HPEL,
HPE length; HSE, secondary external flexus; HSEL, HSE length; Pr.I,
Prism I; Pr.II, Prism II; PW, posterior width. We incorporate new mea-
surements, LPr. I, length of the Pr.I; LPr.II, length of Pr.II
?Hydrochoeropsis wayuu
Tooth HPL/AW HSEL/PW AP AW PW HPEL HSEL IPML (PI) IPML (PII) LPr.1 LPr.II
MUN STRI-12,846 M1 0,54 0.43 6,4 5,55 6,35 3 2,7 3,3 3,7 2,8 2,45
M2 0,47 0.39 6,1 5,9 6,4 2,8 2,5 3,7 4 2,8 2,55
M3 29,05
MUN STRI-16,233 P4 0,54 0,4 13,6 8,4 9,15 4,5 3,7 4,5 7,3 7,1 5,2
M1 0,47 0,36 10 9,6 10,3 4,5 3,7 5,65 6,7 5,3 4,2
M2 0.46 0.38 9,6 10,2 10,5 4,7 4 5,6 7,05 5,05
MUN STRI- 16,438 M1 0,41 0,33 8 7,8 7,95 3,2 2,65 5,2 5,9 4,05 3,45
M2 0,5 0,36 7,9 8,0 8,5 4 3,1 5,3 5,8 4,6 4
MUN STRI- 37,602 p4 6<
Table 2 Skull measurements of ?Hydrochoeropsis wayuu, new
species. PWIF, posterior width of incisive foramen; AZR, rostral with
at the anterior margin of the anterior root of the zygomatic arch; OMS,
width between the anteriormost points of the scars marking the origin of
the masseter superficialis muscle; RWP4, rostral width at the level of P4,
measured at the alveolar margin of Pr.I; PZR, rostral width at the
posterior margin of anterior root of the zygomatic arch; RWM2, rostral
width at the level of M2, measured at the alveolar margin of Pr.II; RL,
distance between posterior margin of the incisive foramen and P4; P4-
M1, antero-posterior length from the P4 to the M1
?Hydrochoeropsis wayuu
Specimen PWIF AZR OMS RWP4 PZR RWM2 RL P4-M1 P4-M2 RWM2/
RWP4
PZR/
RWP4
AZR/
P4-M1
RWP4/
P4-M1
PZR/
P4-M1
RWM2/
P4-M1
MUN STRI-16,233 3,65 17,5 24,3 16 32,8 42,95 18,35 25,25 35,2 2,05 2,68 0,69 0,63 1,30 1,70
MUN STRI-16,438 3 21,4 26,9 18,9 31,4 39,1 13,9 25,6 33,1 1,66 2,07 0,84 0,74 1,23 1,53
MUN STRI-12,846 1,4 19,9 15,9 12,8 18,2 21,6 7,9 18,5 25,3 1,42 1,69 1,08 0,69 0,98 1,17
J Mammal Evol
Distribution and age. —Uquía Formation, Uquía, Jujuy
Province, late Pliocene (Reguero et al. 2007; see also
Deschamps et al. 2013). Ware Formation, the Guajira
Peninsula, northeast Colombia, Piacenzian (Hendy et al.
2015; Moreno et al. 2015).
?Hydrochoeropsis wayuu, New Species
Holotype. — MUN STRI-12,846, maxilla fragment with
left and right M1–M3.
Paratype. —STRI-37,602, a left isolated p4 broken.
Etymology.— Named after the Wayúu, indigenous people
of the Guajira Peninsula in whose territories the specimens
were found.
Referred material. — MUN STRI-16,233, maxilla frag-
ment with left and right P4–M2; MUN STRI-16,438, maxilla
fragment with right M1–2; MUN STRI-34,315, a left femur.
Diagnosis.—Caviidae, diagnosed by the following unique
combination of characters: euhypsodont, and heart-shaped
cheek teeth; p4 with three lobes and complex, and P4 with
two lobes as in Cardiatherium, Hydrochoerus, Neochoerus,
Hydrochoeropsis dasseni, and Phugatherium; H.F.I.
completely crossing the tooth, differing from Cardiatherium
in which the H.F.I. extends beyond the transverse midpoint of
the crown but not splitting it; p4 with C3 as in H. dasseni,
Cardiatherium chasicoense, and Phugatherium, and differing
from Hydrochoerus and Neochoerus in which the h.2i. is be-
hind the apex of the h.f.e.; h.2i and h.3i. equally deep as
H. dasseni , but differing from Hydrochoerus and
Neochoerus in which h.2i. is shallower than h.3i. and its apex
is behind the h.f.e.; h.2i. and h.3i. are parallel as inH. dasseni,
unlike Phugatherium in which they are convergent; h.5i. shal-
low, differing fromH. dasseni in which the h.5i. is deeper; M3
composed of a first prism with H.P.E. and more than ten pos-
terior laminar prisms, differing from that of Cardiatherium,
which has fewer than ten posterior laminar prisms; external
fissures present only in prisms two to five and shallow as in
H. dasseni, unlike Phugatherium which has external fissures
in all laminar prisms and very deep in prisms three to five, and
Hydrochoerus and Neochoerus, in which these fissures are
lacking or are ephemeral; the ventral root of the maxillary
zygomatic arch arises posteriorly to the incisive foramen.
The anterior portion of the palate is relatively flat as in
H. dasseni.
Description and Comparison
As in all hydrochoerines, the cheek teeth are euhypsodont.
The p4 is trilobed, the P4–M2 are bilobed, and the M3 is
multilaminated with cement in the flexus/ids, and the enamel
is interrupted along the labial wall of each lobe (or prism) of
the upper molars (Mones 1991; Vucetich et al. 2005, 2014,
2015b; Deschamps et al. 2007; Pérez et al. 2014).
Lower Premolar The p4 is an isolated and broken left tooth
that lacks its posterior prism (Fig. 3a). This premolar probably
belongs to a young specimen because it is small (Table 1) and
the enamel is not on the entire lingual wall of the tooth (as
occurs in teeth of juvenile-adults of hydrochoerines); instead,
it is slightly interrupted on the lingual wall of the C3 and of the
pr.s.a. The pr.s.a. is smaller than the pr.I, and is oriented
obliquely with the labial apex posteriorly directed (Fig. 3a).
The h.5i. is wide and shallow (Fig. 3a), a condition that differs
from Phugatherium cataclist icum , P. dichroplax ,
Hydrochoeropsis dasseni, Neochoerus, and Hydrochoerus,
in which the h.5i. is narrow and transversely deeper.
Conversely, in P. novum (MMP 236, see Reig 1952;
Vucetich et al. 2014) this fissure is even shallower than in
MUN STRI-37,602, and P. saavedrai lacks the h.5i. The
h.s.e. is deep and wider than in the other species of
hydrochoerines. The pr.I is transversely longer than pr.s.a.,
and the labial apex is transversely oriented (Fig. 3a). It in-
cludes both fissures h.2i. and h.3i. giving rise to a long C3
(Fig. 3a). The fissures are transverse and deep (h.2i. slightly
deeper than h.3i.), reaching up to 50 % of the lobe width
(Fig. 3a) as in P. novum and H. dasseni. In the remaining
species of Phugatherium (including P. dichroplax, see
Vucetich et al. 2015b), these fissures are deeper. The C3 in
P. saavedrai and P. dichroplax is drop-shaped, because the
h.2i. and h.3i. are very long and strongly convergent.
Phugatherium cataclisticum differs from the other species in
having a h.2i. that is much deeper than h.3i. In Neochoerus
and Hydrochoerus, these fissures are also deep but the h.2i. is
included in pr.II (some specimens of Neochoerus have the
h.2i. between pr.I and pr.II.), not in pr.I as in Phugatherium
and H. dasseni. The p4 differs from that of Cardiatherium in
that h.2i. and h.3i. of this genus are shallower and h.5i., if
present, is very shallow. In addition, an h.sn.i. (Vucetich
et al. 2005) is frequent in Cardiatherium.
Upper Cheek Teeth The upper cheek teeth P4, M1, and M2
(Fig. 3b-c) are bilobed and the H.F.I. is completely open on the
labial side, resembling the condition of Phugatherium,
Neochoerus, and Hydrochoerus (although in these genera
H.F.I. of P4 may be closed as individual variation), but con-
trasting with the labially closed H.F.I. in Cardiatherium. The
P4 of the single specimen known of H. dasseni has the H.F.I.
closed, whereas in M1 and M2 this flexus is opened (see
Vucetich et al. 2015b).
Morphologically P4–M2 are similar, though they differ
slightly in size (Table 1). MUN STRI-16,233 is the only spec-
imen that preserves the P4 (Fig. 3b), whereas all specimens
have the M1–2 (Fig. 3c).
The Pr.I of P4 has an anterior wall slightly anteriorly con-
vex with its apex anteriorly directed. The posterior margin is
elongated anterolingually-posterolabially (Fig. 3b), resem-
bling the condition of Hydrochoerus. In the other taxa
J Mammal Evol
(Phugatherium, H. dasseni, and Neochoerus) the Pr.I is more
transverse. In Pr.II the lingual apex is anteriorly directed, the
margin posterolingual and oblique is long, and the anterior
margin is concave in its medial portion (Fig. 3b), resembling
the condition of Hydrochoerus, and contrasting with those of
the remaining hydrochoerines. The H.P.E. of the cheek teeth is
relatively transverse and deep (Fig. 3b), as in H. dasseni,
Hydrochoerus , and Neochoerus . In P. novum and
P. dichroplax, the H.P.E. of P4 is posteriorly oriented. The
H.S.E. is transversely shorter than H.P.E. (similar to
Hydrochoeropsis) and slightly posteriorly oriented (Fig. 3b)
as in P. dichroplax and P. novum. The H.F.I. is relatively wide
and more obliquely oriented than in M1-M2. The lingual por-
tion of the prisms (those without fissure) are more parallel,
thus differing from P. cataclisticum, P. novum, and
P. dichroplax, Neochoerus, and Hydrochoerus. The posterior
portion of the anterior lobe placed between H.P.E. and H.F.I. is
lanceolate-shaped and with a small tip at the labial end
(Fig. 3b). This condition is similar to that of P. dichroplax,
Hydrochoerus, Neochoerus, and H. dasseni, but in this last
species (and in some specimens of Hydrochoerus) the tip
end links both lobes.
TheM1 andM2 aremorphologically very similar to the P4,
but differ in size (Table 1); the lobes are not as strongly direct-
ed forward, and the anterior margin of the Pr.I is straight as in
other hydrochoerines (Fig. 3b-c).
The M3 is preserved only in specimen MUN STRI-12,846
(Fig. 3d,f) and, as in all hydrochoerines, has a first bilobed
prism that is followed by several laminar prisms. In the new
specimen, the first lobe has the anterior margin slightly ante-
riorly convex (Fig. 3d,f). Moreover, the first lobe has the
H.P.E. deep and slightly posteriorly oriented; the orientation
of this fissure is variable between transverse and slightly pos-
terior within the species. The posterior area of this lobe
(Fig. 3d,f), delimited by the H.P.E. and the posterior margin,
is lanceolate-shaped with the major apex transversely orient-
ed, and a sharp labial end. This area is variable in the extension
and orientation of their apices among hydrochoerines. The
new specimen has the same condition as in P. dichroplax
and H. dasseni, and contrasts with that of Neochoerus and
P. cataclisticum in which labial end is not sharp. In
Hydrochoerus the lanceolate area is posteriorly oblique and
the labial end is strongly sharp, and in P. novum the minor
apex is wider than in other species, giving a less lanceolate
shape.
The hydrochoerine of the Guajira Peninsula has 13 poste-
rior laminar prisms in the M3 (Fig. 3d,f). The presence of
more than ten laminar prisms in this molar is a condition
shared with Phugatherium (14 to 18), H. dasseni (13),
Hydrochoerus (10–14), and Neochoerus (13–17), whereas
Cardiatherium has fewer than ten (Vucetich et al. 2014,
2015b). The first eight laminar prisms have the lingual end
posteriorly oriented and relatively sharp, while the last prisms
have a rounded lingual end. The last two laminar prisms are
transversely shorter and the lingual end is not posteriorly ori-
ented. In the hydrochoerine of the Guajira Peninsula, a
Fig. 3 ?Hydrochoeropsis wayuu,
new species. aMUN STRI-
37,602 (syntype) left fourth pre-
molar; bMUN STRI-16,233
maxilla fragment with left and
right P4-M2; cMUN STRI-
16,438 maxilla fragment with
right M1-M2; d-f STRI 12846, d
maxilla fragment with left and
right M1-M3, eM1-M2 detail, f
M3 detail. Scale bar: 1 cm
J Mammal Evol
shallow external fissure is present on the labial wall of the first
five laminar prisms, resembling the condition of H. dasseni,
whereas in Phugatherium these external fissures are present in
all laminar prisms, some of them being very deep (3–6 in
P. cataclisticum , 3–4 in P. saavedrai , and 4–5 in
P. dichroplax).
Maxilla Only three maxillary fragments represent the skull
(MUN STRI-12,846, MUN STRI-16,233, and MUN STRI-
16,438). In ventral view (Fig. 3b-c), the anterior margin of the
maxillary palatal process is broken but preserves the posterior
border of the incisive foramen, which is anteriorly concave
(Fig. 3c). The area delimited between the incisive foramen
and P4 is anterodorsally-posteroventrally oblique (as in other
hydrochoerines), the anterolateral face is anteriorly concave,
and its medial margin converges with its counterpart, forming
the suture of both maxillae as a slight (Fig. 3c) or developed
ridge (Fig. 3b). This ridge extends posteriorly, it narrows be-
tween the P4s, and at the level of M1 it widens up to the
posterior contact with the palate (Fig. 3b-c). At both sides of
the medial suture, there is a groove relatively deep and as wide
as the ridge (Fig. 3b-c). The ventral surface of the maxilla,
between the groove and the toothrow, is narrow at the level of
P4 and becomes wider posteriorly, as in other hydrochoerines.
The posterior margin of the maxillary palatal process is broken
but the posterior border of the palatal foramen can be observed,
and is posteriorly concave (Fig. 3b-c). These palatal foramina
are located at the posterior end of the M2, the same position as
in Neochoerus and Hydrochoerus. The dental series converges
anteriorly, the area between right and left P4 is very narrow, and
the lingual apices of the Pr.I of both premolars are very close
(Fig. 3b-c). The rostrum measured at the level of the anterior
zygomatic root and at the level of the P4 is considerably
narrower than in H. dasseni and Neochoerus, and relatively
similar to juvenile specimens of P. novum (Table 2).
The maxillary zygomatic process has preserved only the
anterior root of the zygomatic arch, the anterior margin of
which arises anterior to the P4, and posterior (or at the same
level) to the incisive foramen (Fig. 3b-c). This condition re-
sembles that of Phugatherium, Hydrochoerus, Neochoerus,
and some species of Cardiatherium, but differs from that of
H. dasseni in which the ventral root of the zygomatic arch
arises anterior to the incisive foramen. The anterior root of
the zygomatic arch is oblique anteromedially-dorsolaterally
(only preserved in MUN STRI-16,233; Fig. 3b), resembling
the condition of P. novum, and contrasting with that of
Hydrochoerus and Neochoerus in which the anterior root is
lateromedially straight and then it directs posteriorly. On the
ventral surface of the zygomatic arch, there is a notch for the
attachment of the m. masseter superficialis (Fig. 3b-c) that
begins anterior to the P4 and extends posteriorly up to the
posterior wall of P4. This notch is very large, occupies most
of the surface of the anteroventral root of the zygomatic
process, and is oval-shaped (with its major axis oriented
anteroposteriorly). This condition resembles that of
Phugatherium and H. dasseni and differs from that of
Hydrochoerus and Neochoerus in which the notch is
anteroposteriorly shorter.
Postcranium Only one postcranial element, a complete and
well-preserved left femur (Fig. 4), was found at the same
locality and is tentatively assigned to the same species.
The femur is straight, but slightly medially concave in the
proximal portion (Fig. 4). Themaximum length (measured from
the greater trochanter to the end of the distal head) and the
maximum width of the diaphysis (measured from the medial
margin to the neck) are shorter than in Hydrochoerus (Table 3).
The proximal portion of the femur preserves the head,
neck, greater trochanter, t rochanter ic fossa, and
intertrochanteric crest (Fig. 4a-c). The femoral head is placed
medially and the greater trochanter laterally in the proximal
portion of the femur. The femoral head is hemispherical and
has a distinct neck, which is proportionally larger than that of
Hydrochoerus (Table 3). The dorsal surface between the head
and the greater trochanter is dorsally concave (Fig. 4a-b), and
wider than inHydrochoerus. The medial margin of the greater
trochanter is straight and vertical (Fig. 4a-b), contrasting with
the condition ofHydrochoerus in which this margin is straight
and oblique ventromedially-dorsolaterally. The greater tro-
chanter in ?H. wayuu has a dorsolateral surface that is dorsally
convex and laterally slightly convex (Fig. 4a-b), resembling
the condition of Hydrochoerus, but in this species the greater
trochanter is more developed. In anterior view, the dorsolateral
border of the greater trochanter forms a ridge that is developed
up to the level of the femoral neck (Fig. 4a). In posterior view,
ventral to the greater trochanter and medially opened is the
trochanteric fossa, which is wide and ovoid-shaped with its
major apex dorsoventrally oriented (Fig. 4b-c), similar to the
trochanteric fossa of Hydrochoerus. This fossa is limited
posterolaterally by the intertrochanteric crest, which is some-
what deteriorated in the femur of the ?H. wayuu (Fig. 4b-c).
Distal to the trochanteric crest is the linea aspera (Fig. 4a-c).
The distal portion of the femur consists of the following
elements: medial and lateral condyles, trochlea, medial and
lateral epicondyles, and intercondylar fossa (Fig. 4a-c). In an-
terior view, the trochlea is an anteroventrally concave fossa,
dorsoventrally elongated, and delimited by the medial and
lateral epicondyles (Fig. 4a). The dorsal margin of this fossa
is dorsally convex and the medial and lateral epicondyles are
laterally flat. The trochlea of the femur is wider than in
Hydrochoerus. In posterior view, the medial and lateral con-
dyles are strongly convex on the entire surface, and between
them, the intercondylar fossa has a straight dorsal margin
(Fig. 4b).
Between the proximal and distal portions, the diaphysis is
slightly anteriorly and posteriorly convex (Fig. 4a-c). The
J Mammal Evol
linea aspera is on the lateral margin of the diaphysis and is
dorsally extended up to the greater trochanter, but not in con-
tact (Fig. 4a-c).
Phylogenetic Analysis
The phylogenetic analysis resulted in 136 most parsimonious
trees (MPTs) of 3244 steps. Caviidae shows a basal polytomy
in the strict consensus (Fig. 5a), because the fragmentary fossil
Microcardiodon huemulensis takes different positions within
this clade in the MPTs. The alternative positions of this unsta-
ble taxon do not affect the monophyly of Hydrochoerinae.
However, the strict consensus does not reflect the affinities
between the three main clades of Caviidae. When the unstable
taxon is ignored from the MPTs (Pol and Escapa 2009), the
reduced consensus retrieves as a monophyletic group
Caviinae, Dolichotinae, and Hydrochoerinae, and these last
two clades as sister groups (Fig. 5b).
?Hydrochoeropsis wayuu is the sister taxon of H. dasseni
and nested among the largest hydrochoerines in all MPTs
(Fig. 5b, node H). Only one unambiguous synapomorphy
supports its position: h.2i. and h.3i. parallel to each other
(character 83[0]). This clade is the sister group of
Phugatherium (Fig. 5b, node I), which is supported by one
unambiguous synapomorphy: first five laminar prisms of M3
with deep external fissures (c. 117[2]). The clade of the largest
hydrochoerines (Hydrochoeropsis + Phugatherium; Fig. 5b,
node G) is supported by two unambiguous synapomorphies:
Fig. 4 MUN STRI-34,315, left
femur. a anterior view; b posterior
view; c medial view.
Abbreviations: d, diaphysis; fh,
femoral head; fn, femoral neck;
ft., femoral trochlea; gt, greater
trochanter; ic, intertrochanteric
crest; la, linea aspera; lc, lateral
condyle; le, lateral epicondyle;
mc, medial condyle; me, medial
epicondyle; tf, trochanteric fossa.
Scale bar: 1 cm
Table 3 Femoral measurements
of ?Hydrochoeropsis wayuu, new
species and Hydrochoerus
hydrochaeris (in millimeters)
?Hydrochoeropsis wayuu
MUN STRI-34,315
Hydrochoerus hydrochaeris
FMNH P 60152
Proximo-distal length 173 210
Maximum width of diaphysis 21 27
Femoral head 18 30
Neck of femoral head 13,15 17
Relation: neck/ femoral head 0,52 0,72
J Mammal Evol
anteroposterior length of the upper diastema equal to or longer
than the molariform series (c. 37[0]) (and h.2i. deeper than
h.3i. (c. 82[0]). This clade is the sister group of Neochoerus
and extant capybaras (Hydrochoerus).
The close affinities between Hydrochoerus and Neochoerus
(Fig. 5b, node I) are supported by four unambiguous synapo-
morphies in all MPTs: posterior extension of the root of the
lower incisors extending up to the level of the anterior lobe of
Fig. 5 a Strict consensus of 136 most parsimonious trees
(Length = 3244) resulting from the parsimony combined phylogenetic
analysis of morphological and molecular dataset using TNT; b Caviidae
with the monophyletic three main lineages: Caviinae, Hydrochoerinae,
and Dolichotinae in the reduced consensus ignoring the unstable and
fragmentary fossil Microcardiodon huemulensis. The numbers in bold
indicate Bremer indices, numbers in italics represent absolute Jackknife
values, and numbers in gray represent GC Jackknife values
J Mammal Evol
Table 4 Bodymass estimates for ?Hydrochoeropsis wayuu. %PE : average absolute percent prediction error. Equation parameters according toMillien
and Bovy (2010: Table 1)
Measurement (mm) r ^ 2 Intercept Slope Standard error % PE Body mass (kg) Mass - PE (kg) Mass + PE (kg)
Femur length = 173 0.86 -1.964 2.825 0.240 48.59 23 12 34
Femur diameter = 21 0.84 0.903 2.635 0.257 47.45 24 13 35
Fig. 6 Temporal and geographic distribution of the most derived
hydrochoerines (†Cardiatherium, †Phugatherium, †Hydrochoeropsis,
†Neochoerus, and Hydrochoerus) from the PBDB. The shaded areas
correspond to the distribution of the two extant species Hydrochoerus
hydrochaeris (Blue) and Hydrochoerus isthmius (Red). Distribution of
extant taxa taken from IUCN (International Union for Conservation of
Nature) 2008. ?Hydrochoeropsis wayuu is indicated by a green square
J Mammal Evol
m1 (c. 20 [4]); h.2i. placed in pr.II of complex p4 (c. 79[1]),
external fissure in pr.II of the complex m3 more than 75 % of
transverse diameter (c. 105[1]), and very superficial or absent
external fissures in the laminar prisms of M3 (c. 116 [0]).
The unambiguous synapomorphies that support the close
relationships between the recent capybaras and the largest
hydrochoerines (Fig. 5b, node H) include the transverse ex-
tension of H.F.I. and h.f.e. completely crossing the teeth (c.
99[3]) and more than ten laminar prisms in the M3 (c. 114[5]).
Cardiatherium chasicoense is the sister group of the more
derived and largest hydrochoerines (Fig. 5b, node G) and this
position is supported by seven unambiguous synapomorphies
(Supporting Information S3).
Body Size Estimate
According to the femoral measurements, ?H. wayuu had a
body mass of ~23–24 kg, with a margin of error ranging from
12 kg to 35 kg (Table 4). It is noteworthy that the femur (MUN-
STRI 34315) does not belong to a young individual, as it has
the distal and proximal epiphysis completely closed (Fig. 4).
Discussion
Taxonomic status of ?Hydrochoeropsis wayuuAccording to
the tooth morphology and the results of the phylogenetic anal-
yses, the new hydrochoerine of the Ware Formation is tenta-
tively assigned to the genus Hydrochoeropsis, because it is
closely related to H. dasseni in all MPTs (see Phylogenetic
Analysis). Here, we propose that the new specimen should be
assigned to a new species for its unique combination of char-
acters (see Diagnosis). However, we are cautious about its
generic assignment because support values in the phylogenetic
analysis are low, and with only one extra step the relations
between Phugatherium, H. dasseni, and ?H. wayuu are unre-
solved (Fig. 5b). This is due mainly to the fragmentary nature
of the remains, which limits information about the new spe-
cies. ?Hydrochoeropsis wayuu is undoubtedly a derived
hydrochoerine because it shares seven synapomorphies with
Cardiatherium , Phugatherium , Hydrochoeropsis ,
Neochoerus, and Hydrochoerus (Online Resource 3).
Although the lower premolar (MUN STRI-37,602) is relative-
ly juvenile (because of its small size) and lacks pr.II, it has
some characters that separate it from the recent capybaras,
Hydrochoerus, and the extinct Neochoerus (such as the pres-
ence of h.2i. in the pr.I), but resemble the condition of
H. dasseni and Phugatherium (see Phylogenetic Analysis).
Significance of Pliocene Capybaras in the Guajira
Peninsula The subfamily Hydrochoerinae is recorded from
the middle Miocene in La Venta Colombia (Vucetich et al.
2015a) and in Patagonia (Vucetich and Pérez 2011). During
the early late Miocene of temperate South America, the most
basal genera of hydrochoerines (Procardiomys, Cardiomys,
Xenocardia; Pérez et al. 2014; Vucetich et al. 2015a, b), and
the derived Cardiatherium chasicoense (Deschamps et al.
2007, 2013) are recorded. From this time, the fossil record
of hydrochoerines is abundant and relatively continuous, re-
cording several species ofCaviodon and Cardiatherium in the
late Miocene (Rovereto 1914; Candela 2005; Vucetich et al.
2005, 2010; Deschamps et al. 2009, 2013). Cardiatherium is
present during the late Miocene, mainly distributed in temper-
ate South America, but is also recorded in tropical South
America (Figs. 6,7; Online Resource 4 contains all the
individual records used for this analysis). A few late
Miocene specimens of Phugatherium (Fig. 6; Supporting
Information S4) have been reported in Argentina (Bondesio
Fig. 7 Summary of the temporal
and geographic distribution of the
most derived hydrochoerines
(†Cardiatherium,
†Phugatherium,
†Hydrochoeropsis, †Neochoerus,
and Hydrochoerus). Data from
Fig. 6 and Supporting
Information S4. Late Miocene
records of Phugatherium are
probably Pliocene and were
excluded (Vucetich and
Deschamps pers. comm.)
J Mammal Evol
1975; Deschamps et al. 2013). However, these specimens are
from the upper levels of the Ituzaingó Formation, and would
correspond to the early Pliocene (Vucetich andDeschamps pers.
comm.). The most derived capybara clade (Phugatherium +
Hydrochoeropsis + Neochoerus + Hydrochoerus) is mostly
known from high latitudes, and they have not been yet recorded
in late Miocene sediments (Figs. 6, 7). Therefore, the lineage
leading to them would have arisen within this time interval
(Fig. 7). Because Cardiatherium is present in both temperate
and tropical latitudes during the late Miocene, it is still uncertain
whether the largest and recent hydrochoerine lineages originated
in temperate South America and rapidly migrated toward trop-
ical latitudes, or vice versa (Fig. 7).
Femoral body size estimates yielded a body mass of ~23–
24 kg for ?H. wayuu, comparable to the lesser capybara,
H. isthmus (~28 kg) and smaller than H. hydrochaeris (35–
65 kg). The two extant species differ in size and craniodental
morphology (Aeschbach et al. in press). Hydrochoerus
hydrochaeris shows intraspecific size and cranial shape differ-
ences across its geographical distribution, increasing in mass
with increasing latitude (Mones and Ojasti 1986; Moreira
et al. 2013; Aeschbach et al. in press). ?Hydrochoeropsis
wayuu is smaller than Phugatherium (Vucetich et al. 2014)
and Neochoerus; for the latter, body mass estimates range
from 110 kg (Vizcaíno et al. 2012) to ~200 kg (Ghizzoni
2014). The relatively small size of ?H. wayuu suggests a
higher body size disparity and geographical variation within
the clade since the Pliocene.
During the Pliocene (5.3 to 2.7 Ma) the diversity of
hydrochoerines decreased and their geographical range
showed a dramatic change, with the first migration toward
Central America and temperate North America (Figs. 6-7),
during the GABI (Woodburne 2010). This initial dispersal
across the Panamanian Isthmus could have been facilitated
by the almost full emergence of the Isthmus by 10 Ma
(Montes et al. 2015), and it is coetaneous with a significant
wave of terrestrial dispersals across the Isthmus of many dif-
ferent clades at 6 Ma (Bacon et al. 2015). Despite the abun-
dance of fossil mammals in North America and in temperate
South America, the record from tropical South America is still
scant and the information available to document the migration
pathways is scarce (Carrillo et al. 2015). Nevertheless, given
that the land connection occurs in the tropics, it is expected
that many of the taxa that participated in the interchange
or their close relatives inhabited tropical areas (Webb 1991).
The Pliocene record of hydrochoerines (the largest capy-
baras) consists of Phugatherium, which is recorded in south-
ern South America (Deschamps et al. 2013; Vucetich et al.
2014, 2015b) and whose presence in the Pliocene of North
America was recently corroborated with P. dichroplax
(Vucetich et al. 2015b), and H. dasseni from the Uquía
Formation (Kraglievich 1930). There is also one report from
the late Pliocene to early Pleistocene of Grenada (Lesser
Antilles, MacPhee et al. 2000) that corresponds to
Hydrochoerus gaylordi, but this occurrence is controversial
and the specimen needs to be re-examined (see Vucetich
et al. 2012). In northern South America, fragmentary remains
from the Pliocene of the San Gregorio Formation (Venezuela)
tentatively assigned to Cardiatherium also need to be re-
examined (Vucetich et al. 2010, 2015b). These remains consist
of small tooth fragments with the lobes still united, a diagnostic
character of Cardiatherium, but also of young individuals of
more derived hydrochoerines (Vucetich et al. 2014). Hence,
taking into account the age of the fossil-bearing levels and
the geographical proximity, these remains may represent juve-
niles of ?H. wayuu. Additional caviomorphs from San
Gregorio include the hydrochoerid Caviodon, the octodontid
Marisela gregoriana, and the neoepiblemid Neoepiblema
(Vucetich et al . 2010). Of these, neoepiblemids
(Neoepiblema and Phoberomys) are also recorded in the late
Miocene deposits of the Urumaco Formation (Sánchez-
Villagra et al. 2003; Carrillo and Sánchez-Villagra 2015).
During the late Pliocene and Pleistocene (2.7 to 0.01 Ma)
diversity of the Hydrochoerinae declined, with only two clades
recorded, Neochoerus/Hydrochoerus and Phugatherium. While
Neochoerus/Hydrochoerus were widely distributed in tropical
and temperate South America, Central America, and North
America, Phugatherium is restricted to temperate North
America (Guanajuato, Mexico; Arizona, USA). The recent cap-
ybaras Neochoerus and Hydrochoerus are recorded in the
Pleistocene of several localities of South America (Ameghino
1902; Soibelzon et al. 2005; Tonni et al. 2009; Kerber and
Ribeiro 2012; Deschamps et al. 2013) and North America
(Mones 1991). The validity of some species of Neochoerus
andHydrochoerus (e.g., N. aesopi, H. gaylordi) is controversial
(see Mones 1991; Baskin and Thomas 2007; Morgan 2005,
2008; Vucetich et al. 2015b) and these need a more exhaustive
revision. By the Holocene (10,000 b.p.), only one lineage of
Hydrochoerinae is present (Hydrochoerus), and it is represented
by the two extant species: H. hydrochaeris and H. isthmius
(Figs. 6-7).
?Hydrochoeropsis wayuu from the Ware Formation in the
Guajira Peninsula would be the northernmost hydrochoerine
record from the Pliocene of South America, and the nearest one
to the Panamanian bridge at 3.2 Ma (Moreno et al. 2015). By
that time (late Pliocene) one of the largest capybaras,
P. dichroplax, had already crossed the Isthmus as is evidenced
by its record in Guanajuato (Mexico) and Arizona (USA) dur-
ing the late early to early-late Blancan (Morgan 2008;
Deschamps et al. 2013; Vucetich et al. 2015b). Vucetich et al.
(2015b) indicated that oldest record of P. dichroplax in the late
Pliocene of North America (Guanajuato, Mexico; 3.6 Ma) sug-
gesting that this lineage was present in northern South America
before 3.6 Ma. The presence of ?Hydrochoeropsis wayuu in
Guajira corroborates that the lineage of the largest capybaras
inhabited the low latitudes of South America during the GABI.
J Mammal Evol
Today Hydrochoerus does not inhabit the Guajira
Peninsula, an extremely dry landscape that has a prolonged
dry season (~11 months), is dominated by xerophytic vegeta-
tion, and lacks large rivers or year-round bodies of fresh water.
Capybaras, which depend on water physiologically and for
refuge (Herrera 2012) require habitats close to water bodies
including marshes, estuaries, swamps, and the banks of rivers
and streams. This suggests that major changes in the land-
scape occurred, leading to the extreme aridification of the
region over the past 2.5–3 Ma.
Acknowledgments We thank François Pujos and Pierre-Olivier
Antoine for inviting us to submit a manuscript for the special issue
(TREMA Symposium on Cenozoic evolution of Tropical-Equatorial
mammals; IPC 4, Mendoza, 2014). Thanks to María Guiomar Vucetich
and Cecilia Deschamps (MLP) for critical comments that enhanced the
quality of this manuscript, and Bruce Patterson for access to Zoology
Collection of FMNH. We are grateful to support from the Smithsonian
Institution, the National Geographic Society, Universidad del Norte, the
Anders Foundation, Gregory D. and Jennifer Walston Johnson, Marcelo
R. Sánchez-Villagra and the Evolutionary Morphology and
Palaeobiology of Vertebrates group at the University of Zurich, the
Swiss National Science Foundation (SNF 31003 A-149605 to M.R.
Sánchez-Villagra), and the National Science Foundation (grant EAR
0957679). Thanks to Carlos Rosero for managing all the logistics in the
field, and to Liliana Londoño and Maria Inés Barreto for administrative
and logistic support. Thanks to the Wayúu community for allowing us
access to their lands and for their support during the field work, the
Colombian National Police (Castilletes base), and all the members of
the field team, in particular F. Moreno, J.W. Moreno, and V. Zapata,
who found the first specimens.
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