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Journal of Human Evolution 50 (2006) 673e686
New platyrrhine monkeys from the Solim~oes Formation(late Miocene, Acre State, Brazil)
Richard F. Kay a,*, Mario Alberto Cozzuol b
a Department of Biological Anthropology and Anatomy, Duke University, Durham NC 27710, USAb Laboratorio de Paleontologia, Museu de Ciencia e Tecnologia - PUCRS, Porto Alegre, RS, Brazil
Received 16 September 2004; accepted 16 January 2006
Abstract
We report here a new fossil primate from the late Miocene of Brazil. The material consists of a lower first molar and a maxilla with P3e4.The fossils were collected in the Solim~oes Formation at the locality of Patos, upper Acre River, Acre State, Brazil. The locality is assigned to theHuayquerian South American Land Mammal Age based on faunal content (late Miocene; dated to between 9 and 6 Ma). The new material is theoldest known occurrence of fossil primates in Brazil and is recognized as a new genus and species, Solimoea acrensis. Solimoea is the oldestknown member of the ateline subfamily, which includes the living genera Ateles, Lagothrix, and Brachyteles. By analogy with the molar struc-tures and diets of extant platyrrhines, Solimoea primarily had a diet of fruit, perhaps similar to that of the spider monkey, Ateles. Two otherprimate teeth described previously from the same formation in Bolivia document the occurrence of alouattines and cebines. One of those spec-imens is a late Miocene representative of the middle Miocene Colombian genus Stirtonia. The other represents one of the largest known plat-yrrhine primates, for which is erected a new primate genus, Acrecebus fraileyi.� 2006 Elsevier Ltd. All rights reserved.
Keywords: Anthropoidea; Platyrrhini; Cebidae; Cebinae; Atelinae; Solim~oes Formation; Miocene; Brazil
Introduction
Fossils vertebrates in the Solim~oes Formation were first re-ported by the middle of the 19th century (Chandless, 1866)and described by Agassiz (1868) as belonging to Mesozoicmarine reptiles. About a century later, Price (1953) reinter-preted the material as a giant alligatorid crocodile. Betweenthose publications, a few reports of Amazonian vertebratescan be found (Gervais, 1876, 1877; Barbosa Rodrigues,1892; Goeldi, 1906; Gurich, 1912; Mook, 1921; Roxo, 1921;Kraglievich, 1930, 1931; Roxo, 1937; Miranda Ribeiro,1938; Paula Couto, 1944). In 1956, G.G. Simpson and L. Priceconducted fieldwork along the Jurua River, Acre State, and itstributaries, and collected a large number of vertebrate
* Corresponding author. Tel.: þ1 919 684 2143; fax: þ1 919 684 8542.
E-mail addresses: [email protected] (R.F. Kay), [email protected]
(M.A. Cozzuol).
0047-2484/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2006.01.002
specimens presently housed in the Departamento Nacionalde Produc~ao Mineral (DNPM, Brazil), Museu Nacional, Riode Janeiro, Brazil, and in the American Museum of NaturalHistory, New York (Price, 1953). The material is of Quater-nary and Tertiary age, although often the age was not clear.A series of papers by Paula Couto and Simpson describedpart of this collection (Paula Couto, 1976, 1978, 1981;Simpson and Paula Couto, 1981; Paula Couto, 1982, 1983a,b).
During the 1970s and up through the 1990s, Los AngelesCounty Museum sent several expeditions to the region (Camp-bell and Frailey, 1984; Campbell et al., 1985, 2000; Frailey,1986). In parallel, during the last two decades, paleontologistsfrom the Universidade Federal do Acre, Brazil, joined recentlyby the University of Rondonia, have collected more than 5,000specimens of vertebrates from the Solim~oes Formation out-crops in Acre State and southern Amazonas State. A signifi-cant portion of these collections have been published inbrief reports or abstracts, Masters theses and Ph.D. disserta-tions, and local journals, many in the Portuguese language,
674 R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
and are not widely cited in recent geologic publications on theTertiary evolution of Amazonia.
Despite the great richness and abundance of primate species inmodern faunas of the southwestern Amazon hydrographicbasindup to 16 sympatric species (Kay et al., 1997)dprimateshave been poorly represented in fossil collections of a centuryand a half. Indeed, up until now, only three specimens of Mioceneprimates have been reported. In his summary of late Miocene andHolocene mammals of the Acre River, Frailey (1986) figured andallocated a single tooth to the procyonid Carnivora. Restudy ofthis specimen indicated it to be a specimen of the primateStirtonia, hitherto known from the middle Miocene of Colombia(Kay and Frailey, 1993). In the same paper, Kay and Fraileydescribed but did not name a further specimen of primate that isnamed in this paper. Finally, Bergqvist et al. (1998) describedan isloated primate talus. These three specimens represent thesum total of our knowledge of primates anywhere on the SouthAmerican continent between about 11.8 Ma in Colombia (Kayand Meldrum, 1997) and the Pleistocene of Bahia, Brazil(Cartelle and Hartwig, 1996; Hartwig and Cartelle, 1996). In viewof this rarity, the description of new primate material discoveredby a recent joint Universidade Federal do Acre/University ofRondonia expedition to the Solim~oes Formation deserves spe-cial attention.
Geology and paleontology
The Solim~oes Formation is of great aerial extent in south-western Amazonia. Sediment cores suggest a maximum thick-ness of 1800 m, although surface outcrops in road cuts andexposed along the banks of the principal rivers in this regionpresent a maximum thickness of 70 to 100 m (Latrubesseet al., 1997). The temporal interval of deposition for the for-mation has been reported as spanning Paleocene to Pleisto-cene. However, recent data indicate that its range may befrom the late early Miocene to the late Miocene (Hoorn,1993, 1994a,b, 1996; Hoorn et al., 1995). In the Acre region,the thickness of the formation is about 800 m, and the outcrops(including the ones containing primates) are considered to beof late Miocene age (Huayquerian SALMA) based on themammalian faunas. Radiometric dates from volcanic ash insediments correlative to the Solim~oes Formation at two Peru-vian localities close to the Brazilian border gave dates of 9.01and 3.12 Ma (Campbell et al., 2001). These dates are congru-ent with the age indicated by the fossil vertebrates, but the pre-cise stratigraphic position of the lower ash is not clear(Campbell et al., 2000).
Latrubesse et al. (1997) interpreted the Solim~oes depositsas being part of a megafan system, with its headwaters inthe Peruvian Andes. The relevant tectonic phase was initiatedin the Bolivian and Peruvian Andes approximately 10� 2 Ma(Jordan et al., 1983; Marshall and Sempere, 1993). The geo-logical interpretation is concordant with the Huayquerianage (w9 to 6 Ma) of the mammalian faunas (Marshall et al.,1983; Flynn and Swisher, 1995). According to this chronol-ogy, the temporal constraints on the age of the primates de-scribed here places them between 5 and 8 myr younger than
primates occurring in the middle Miocene of Columbia (Flynnet al., 1997; Madden et al., 1997) and 9 to 6 myr older thanthose from the late Pleistocene of Brazil (Cartelle andHartwig, 1996; Hartwig and Cartelle, 1996).
The new primate fossils occur in the Solim~oes Formation atPatos, along the upper Acre River (10 � 550 5500 S, 69 � 550 2000
W) in a riverbank cut approximately 38 km upriver from thetowns of Assis (on the Brazilian side) and Inapari (on thePeruvian side) (Fig. 1). The outcrop is visible only in thelow-water season and consists of an intraformational conglom-erate with clasts of clay and silt. It is part of a large paleochan-nel (Fig. 2). The base of the unit is not visible, and its upperpart is covered by vegetation. Several other specimens foundat the same locality and still under study include potamotrygo-nid rays; catfishes of the families Callichthydae, Doradidae,and Pimelodidae; characiform fishes of the family Characidae,crocodiles of the families Alligatoridae and Gavialidae;aquatic turtles; and mammals. Among the latter are marsupialsof the family Didelphidae (cf. Didelphis), xenarthrans of thefamilies Dasypodidae and Glyptodontidae, and sloths. Rodentsare represented mainly by teeth, but some more completespecimens were also recovered. They belong to the familiesCaviidae, Erethizontidae, Dinomydae, Dasyproctidae, andEchimydae. Fragmentary remains of notungulates were alsofound. A faunal composition list from the same locality isprovided by Frailey (1986) and Cozzuol (in press).
Fig. 1. Map showing the position of the Patos locality along the Acre River on
the border between Peru and Brazil, upstream of the town of Assis.
675R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
Fig. 2. The Patos locality along the Acre River: A) at a distance; B) showing the river bank with a stratigraphic profile of the site; C) close-up of the fossil-bearing
conglomeratic layer.
Taxonomic considerations
The monophyly of the extant Atelidae, consisting ofAlouatta (the howler monkey), Ateles (the spider monkey),Lagothrix (the woolly monkey), and Brachyteles (the muriquior woolly spider monkey), is well established from morpho-logical and molecular evidence (Rosenberger, 1979b; Ford,1986; Schneider et al., 1993, 1996; Horovitz, 1999; Horovitzand MacPhee, 1999; Meireles et al., 1999a,b). The familyconsists of two extant clades, the Alouattinae (Alouatta) andthe Atelinae (Ateles, Brachyteles, and Lagothrix). Within atelines,Lagothrix and Brachyteles are sister taxa (Fig. 3).
Fossil occurrences of alouattines are scant. The oldest is thew13.2-myr-old Stirtonia (middle Miocene, Colombia), ofwhich there are two speciesdS. tatacoensis and S. victoriae(Stirton and Savage, 1951; Hershkovitz, 1970; Setoguchiet al., 1981; Kay et al., 1987, 1990). Kay and Frailey (1993)referred an isolated molar from the late Miocene Solim~oesFormation of Bolivia to cf. Stirtonia. Paralouatta, from karstdeposits in Cuba, is either an alouattine (Rivero andArredondo, 1991) or a pitheciine (Horovitz, 1999; Horovitzand MacPhee, 1999; MacPhee and Horovitz, 2004).
The fossil record of atelines consists of two genera andspecies (Protopithecus brasiliensis and Caipora bambuiorum)
676 R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
from karst deposits of Pleistocene or Holocene age in MinasGerias and Bahia States, Brazil (Cartelle and Hartwig, 1996;Hartwig and Cartelle, 1996).
The subfamily Cebinae is represented today by Saimiri andCebus. Molecular evidence suggests that these two taxa di-verged from one another in the early Miocene (Haradaet al., 1995). Cebines specially related to the Cebus cladeare represented only by a single tooth from the late Mioceneof Bolivia (see below). Dolichocebus from the early Mioceneof Argentina is often considered to be a relative of Saimiri(Rosenberger, 1979a, 1982). Others believe it to be a stemplatyrrhine (Hershkovitz, 1982; Kay and Mitchell, 2003;Mitchell et al., 2004). Neosaimiri (¼Laventiana) from themiddle Miocene of Colombia is another Saimiri-like species(Setoguchi et al., 1990; Rosenberger et al., 1991; Takai,1994; Fleagle et al., 1997).
Abbreviations
By convention, upper teeth are designated by capital lettersand lower teeth by lower case letters, viz., P4 and m1. Institu-tional abbreviations are as follows: LACM, Los AngelesCounty Museum vertebrate paleontology collections; UFAC,Universidade Federal do Acre, Rio Branco, Acre State, Brazil.
Systematic paleontology
Order Primates Linnaeus, 1758Semiorder Haplorhini Pocock, 1918Suborder Anthropoidea Mivart, 1864Infraorder Platyrrhini Geoffroy, 1812Family Atelidae Gray, 1825Subfamily Atelinae Mivart, 1865
Solimoea genus nov.
Fig. 3. Maximum parsimony tree for extant Atelidae found by Meireles et al.
(1999a,b) using a combination of g-Globin, e-Globin, RBP, G6PD nuclear
genomic sequences, as well as mitochondrial COII sequences. All nodes
have 100% bootstrap support.
Diagnosis
Solimoea is a large platyrrhine monkey comparable in dentaldimensions and proportions to extant Ateles spp. and Lagothrixlagotricha. The species is autapomorphic among atelines in hav-ing an elongate and narrow m1, and P3e4 with three distinctrootsdtwo buccal and one lingual. Solimoea resembles crownatelines in having the following derived character states (withthe primitive state for Atelidae in parentheses): m1 shearingcrests moderately developed (vs. strong); m1 hypocristidweakly developed (vs. strong); P3e4 hypocones absent (vs.commonly present on one or both teeth); and P3e4 buccal cin-gulum weakly developed (vs. strong). However, Solimoea lacksa number of crown atelid synapomorphies (derived states forcrown Atelinae in parentheses): m1 metaconid posteriorly dis-placed relative to the protoconid (vs. approximately transversein crown atelines); m1 hypoconulid present as a swelling ona lingual terminus of a distal transverse ridge (vs. absent);pre-ento-cristid and postmetacristid fused to form a completelingual wall for the talonid basin (vs. notched lingually).
Etymology
Name derived from the formation and state from which thefossils come.
Solimoea acrensis species nov.
Holotype
Specimen UFAC-LPP 5177, a left lower first molar, col-lected by the joint team of the University of Acre and Univer-sity of Rondonia in September 2002 (Fig. 4A).
Hypodigm
Specimen UFAC-LPP 5178, a maxillary fragment contain-ing right P3e4, collected in September 2000 at the same local-ity as the holotype (Fig. 4B).
Locality
Patos, Upper Acre River, 10 � 550 5500 S, 69 � 550 2000 W,southern Acre State, along the border with Peru. Equivalent toLACM 4611 (Frailey, 1986; Kay and Frailey, 1993).
Diagnosis
Diagnosis same as for genus.
Description
The two known specimens of Solimoea come from the wetscreen concentrate at the locality of Patos (see above). Whilethe two specimens come from two different regions of the den-tition, we allocate them to a single species for several reasons.First, because they come from the same locality and owing to
677R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
Fig. 4. A) Occlusal and lateral photograph of UFAC-LPP 5177 left m1, type specimen of Solimoea acrensis. Mesial is to the left; buccal is to the bottom.
B) Occlusal and lateral photographs of UFAC-LPP 5178, maxilla with right P3-4. Mesial is to the right; buccal is to the top (in occlusal view). The alveolus
on the left is for the mesiobuccal root of M1. C) Occlusal photograph of LACM 134880, type specimen of Acrecebus fraileyi. Mesial is to the right; buccal
is to the top. Scale bar¼ 5 mm.
the general rarity of primates in the Solim~oes Formation, theworking hypothesis was that they belong together. Second,the morphological features of one can be predicted from theother. Specifically, the lower molars have moderate develop-ment of shearing crests (e.g., moderate development of cristidobliqua), while the upper premolars likewise have moderatedevelopment of the crestsdthe preparacrista and postparacristaare short, mesiodistally oriented, and lack supporting conules.Third, the lower molar dimensions and upper premolar dimen-sions are consistent with the specimens coming from the samespecies. Figure 5 is a bivariate plot of lower first molar area vs.upper fourth premolar area in a sample of extant Lagothrixlagotricha from a restricted geographic area. If the proportionsof the upper and lower teeth of Solimoea are similar to those ofLagothrix, the P4 area of specimen #5178 is about as expectedfor the m1 area of specimen #5177.
Lower molar.. The crown of UFAC-LPP 5177 is slightly wornbut well-preserved. The tooth had two widely separated roots.The mesial root is partially preserved, but the distal root islost. The crown is relatively long mesiodistally for its buccolin-gual breadth, and the trigonid is narrower than the talonid
(dimensions are as follows: mesiodistal length, 6.12 mm; buc-colingual breadth of trigonid, 4.51 mm; buccolingual breadthof talonid 4.89 mm). It is characterized by moderate cusp reliefand smooth enamel. The trigonid is two-cusped. The metaconidis quite far distolingual to the protoconid. The trigonid basin is
Fig. 5. Bivariate plot of lower first molar area vs. upper fourth premolar area in
a sample of extant Lagothrix lagotricha from a restricted geographic area.
Solimoea acrensis (filled circle) has a P4 area about as expected for its m1 area.
678 R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
closed lingually by an extension of the paracristid that runs to thebase of the metaconid. The entoconid is large and positionedslightly distal to the hypoconid. The specimen lacks a hypoco-nulid and a postentoconid sulcus. The cristid obliqua connectsto the trigonid wall distolingual to the protoconid and reachesthe distolingually oriented protocristid. The lingual margin ofthe talonid basin forms a complete wall. There is no buccalcingulum.
Upper premolars.. Specimen UFAC-LPP 5178 holds two teeth,the right P3e4, embedded in a fragment of maxilla. A part ofthe alveolus for the root of M1 is preserved (see Fig. 4B). Thefacial plane of the maxilla is worn away so as to reveal thebuccal roots of the premolars. Notably, both P3 and P4 havetwo buccal roots. Including the lingual root visible on the dor-sal surface of the specimen and confirmed by an X-ray, P3 andP4 are three-rooted. The crowns of the teeth are somewhatworn, with the enamel of the protocone and paracone perfo-rated. Dimensions of P3 are: mesiodistal length, 4.13 mm;buccolingual breadth, w5.8 mm; P4 mesiodistal length,4.57 mm; buccolingual breadth, 6.05 mm. The crowns ofboth teeth are oval in occlusal outline, with the buccal sideslightly longer mesiodistally than the lingual side. The mesialocclusal outlines are straight and the distal occlusal outlinesbulge slightly. There are strong paracones and protocones,but metacones are absent. Postprotocristae are well developedand sweep distally and then buccally to rim the talon basins.Neither tooth has a hypocone. The buccal crests (pre- andpostparacristae) are short, mesiodistally oriented, and lacka parastyle or metastyle. The buccal surfaces are smooth andlack a cingulum.
Phylogenetic position of Solimoea
The phylogenetic position of Solimoea was examined usingPAUP version 4.0b10 (Swofford, 2002). The characters relateto upper premolar (P3 and P4) and lower molar (m1 and m2)anatomy. We evaluated a total of 57 molar and premolar charac-ters that are parsimony-informative within Anthropoidea asa whole (Kay et al., 2004). Among the atelids used in this study,we found 25 characters that exhibit no taxonomic variation andso were set aside. We found a further seven characters in the dataset to be parsimony-uninformative because they are autapomor-phies of terminal taxa. This left 25 parsimony-informative char-acters upon which to base our phylogenetic observations. A listof all characters and their states (whether used or not) is given inAppendix I to ensure comparability with larger published datamatrices of Anthropoidea (Kay et al., 2004).
The character-taxon matrix (Appendix II) consists of extantatelids (three species of Alouatta, Ateles geoffroyi, Brachytelesarachnoides, Lagothrix lagotricha), as well as Stirtonia tata-coensis (middle Miocene, Colombia) and the Solimoea speci-mens (in composite). We do not include observations on thedentitions of Protopithecus brasiliensis and Caipora bambuio-rum because they have not been fully described. Data for theextant taxa are complete. However, some characters cannot bescored. For example, the position of the m1 paraconid relative
to protoconid and metaconid is scored as ‘‘missing’’ in taxawhere a paraconid is absent.
Four sets of options in PAUP were employed in the analy-sis: the characters are scaled1 or unscaled, and ordered ora mixture of ordered and unordered. The tree-bisection-reconnection (TBR) branch-swapping algorithm of PAUPwas selected. For each set of comparisons, starting trees wereobtained via stepwise addition with a random additionsequence with one tree held at each step. The search processwas replicated 1000 times.
Following the recommendation of Springer et al. (2001)concerning the use of the ‘‘Constraints Backbone’’ option ofPAUP, we established a ‘‘molecular scaffold’’ upon which toanalyze the premolar and molar characters. Springer et al.argued that clades established by maximum parsimony analy-sis of molecular data should be assumed to depict a cladeaccurately if they receive �90% bootstrap support. In thiscase, molecular data establish the phylogenetic relationshipsamong extant atelids with a high degree of probability. Indeed,Meireles et al. (1999a,b) reported 100% bootstrap support forthe nodes in Figure 3.
Under the ‘‘backbone’’ constraint, extinct taxa are uncon-strained and can move about on the molecular scaffold. Tree root-ing assumes that Stirtonia tatacoensis (and S. victoriae, notanalyzed) is the sister taxon of the clade of extant Alouatta species(Hershkovitz, 1970; Setoguchi et al., 1981; Kay et al., 1987, 1990;Fleagle et al., 1997; Horovitz, 1999). This outgroup rooting is con-sistent with the molecular rooting. In a further set of runs, bootstrapsupport values were obtained under each set of assumptions.
Results of all analyses are summarized in Figure 6 andTable 1. Three of the four assumption sets yield precisely thesame result: Solimoea fits at the base of the clade ((LagothrixþBrachyteles) Ateles). Stirtonia tatacoensis falls at the base of theAlouatta clade in three of the four analyses; in the fourth,it clusters as the sister-taxon to Brachyteles2 (Fig. 6). Three offour bootstrap runs place Solimoea in the same position asdepicted in Figure 6. Under various assumption sets, Solimoeaclusters with Ateles, Lagothrix, and Brachyteles between 57%and 86% of the time. In run 1, Stirtonia clusters with extantatelines by virtue of its similarities to Brachyteles; in all otherruns, it falls with Alouatta. Based on these findings, we acceptthe interpretation presented in Figure 6.
Character evolution
The morphological characters analyzed here, when mappedonto the phylogeny in Figure 6, yield the following distribu-tion.3 Crown Atelinae and Solimoea differ from alouattines
1 If a character has two states among the taxa used in this study, a shift from
one state to another is given an arbitrary weight of 100. If it has three states
the weight for each step is assigned a value of 50 and if there are 4 states
the step-weight is 33.2 Brachyteles and Alouatta exhibit striking convergence in the dentition and
masticatory system (Zingeser, 1973; Kay and Anthony, 1991).3 Some variation occurs in these characters within species of Alouatta; see
Appendix II.
679R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
(Alouatta and Stirtonia) in a number of upper premolar andlower molar character states, some or all of which maybe atelid synapomorphies. On m1e2:
1) trigonid breadth is greater than or equal to the breadth of thetalonid (vs. a narrower trigonid in Alouatta) (Character 3);
2) the m1 metaconid is approximately transverse to the pro-toconid (vs. posteriorly displaced) (Character 12) (exceptin Brachyteles; see footnote2);
3) The m1 and m2 lack a postentoconid sulcus (vs. present)(Character 19);
4) the m1 hypoconulid is absent (vs. present as a swelling on thelingual terminus of the transverse distal ridge) (Character 20);
5) the m1e2 shearing crest development is moderate to weak(vs. strong) (Character 23) (except in Brachyteles);
6) on m1e2, the cristid obliqua reaches the trigonid wall ata point just distal to the protoconid (vs. being directedmore lingually) (Characters 24, 25) (except in Brachyteles);
7) the m2 cristid obliqua connects with the protocristid (vs.running to the base of the distal trigonid wall) (Character27) (except in Brachyteles);
8) the m1e2 hypocristid is weakly developed (vs. strong)(Character 29) (except in Brachyteles);
Fig. 6. Maximum parsimony tree resulting from three of four phylogenetic
analyses.
9) lingual crests running mesially from the entoconid anddistally from the metaconid are notched lingually (vs.fused, forming a complete lingual wall for the talonidbasin) (Character 30);
10) on m1e2, the hypoflexid is moderately deeply incised (vs.deeply incised) (Characters 36, 37) (except in Brachyteles);
11) m1 length is slightly longer than the breadth (vs. >16%longer) (Character 39) (except in Brachyteles).
While it shares the features listed above with crown ate-lines, Solimoea lacks several apparent synapomorphies of theupper premolars of extant (¼crown) atelines. Crown atelines,except as noted, have the following traits:
1) P3e4 generally have one root (resembling a ‘‘Fig. 8’’ incross section; except in Brachyteles) (vs. three roots inSolimoea and two or three roots in some P4s of Alouatta)(Characters 42, 43);
2) P3e4 hypocones are absent (vs. commonly present on oneor both teeth) (Character 49);
3) P3e4 buccal cingulum is weakly developed (vs. strong;except in Brachyteles) (Character 57).
Based on comparisons with a variety of outgroups, wereconstruct characters 19, 36, and 37 as synapomorphies ofAlouattinae (including Stirtonia). Thus, the last commonancestor of crown atelines (although not necessarily all thedescendants) possessed the derived states of characters 3, 12,20, 23, 27, 29, 30, 42, 43, 49, and 57. Of those derived statesof crown atelines, Solimoea has fourd23, 29, 49, and 57dbutretains the primitive atelid states for 12, 20, 30, 42, and 43.Data for characters 3 and 27 are missing for Solimoea. Thus,we infer that Solimoea is a stem ateline.
Adaptations of Solimoea
Body size
Determination of body weight for Solimoea is based on itsmolar occlusal area, 29.9 mm2. From body weights of femalesof 15 platyrrhine species found in the literature and molarareas of the same species, Kay et al. (1998) derived the follow-ing least-squares regression with an r2 of 0.935:
ln female body weight¼ ln m1 areað1:565Þ þ 3:272
Table 1
Summary of phylogenetic analyses (all runs utilize the atelid molecular scaffold in Figure 3)
Run Characters
(n)
Parsimony
informative
characters (n)
Taxa
(n)
Weight
scheme
Order Maximum
parsimony
trees (n)
Tree
length
CI RI RCI Bootstrap support
for Solimoea with
extant atelines
All taxa, all characters 57 25 8 Scaled Some characters
ordered
1 4916 0.60 0.41 0.24 86%
All taxa, all characters 57 25 8 Equal weights Some characters
ordered
1 61 0.61 0.42 0.25 58%
All taxa, all characters 57 25 8 Scaled unordered 1 4883 0.60 0.39 0.23 86%
All taxa, all characters 57 25 8 Equal weights unordered 1 60 0.62 0.40 0.24 57%
680 R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
From this equation, the body weight of Solimoea was esti-mated as 5.4 kg. Similar results are obtained from a formulapublished by Conroy (1987) based on both catarrhines andplatyrrhines: mean¼ 6.01 kg (range: 2.5 kge15.6 kg). Thismakes Solimoea about the same size as the woolly monkey(Lagothrix) or spider monkey (Ateles).
Molar shearing and diet
The functional design of the cheek teeth of platyrrhinesreflects adaptations in response to the physical properties ofthe foods the species eats (Kay, 1975, 1984; Rosenberger andKinzey, 1976; Strait, 1991; Anthony and Kay, 1993; Fleagleand Kay, 1997; Meldrum and Kay, 1997). These differencesare quantified by examining the development of the shearingcrests on the molars relative to molar size and expressed as aresidual percentage, the ‘‘shearing quotient’’ (SQ) (for full details,see Kay et al., 2002). In Figure 7, SQs for all 16 extant genera ofplatyrrhines are broken down by dietary preference. Speciesthat eat considerable amounts of fibrous foods, such as leaveshigh in cellulose (Alouatta, Brachyteles) or chitinous insects(Saimiri, Callimico), have well developed molar shearing crests.In contrast, species that feed on less fibrous soft fruits (Ateles,Callicebus) or tree gum (Callithrix, Cebuella) tend to have rela-tively flatter molars with shorter, more rounded shearing crests.
The SQ of Solimoea is approximately �5%,4 placing itwithin the range of extant platyrrhine species that eat primarilyfruit and some leaves. In this respect, molar shearing inSolimoea is not significantly different from that of the mostfrugivorous extant atelid, Ateles geoffroyi (mean¼�4.35%;n¼ 10). Lagothrix, which has a diet of fruit and leaves, hasmore shear at þ0.16%; Alouatta species are more folivorous andrange from þ5.6% to þ10.1%. Brachyteles is perhaps themost folivorous of all extant atelids and has an SQ of þ15.5%.
Notes on other primates from the Solim~oes Formation
Kay and Frailey (1993) described a large upper molar withcebine affinities (LACM 134880) collected in the 1970s byFrailey and Campbell along the Rio Acre, downstream fromthe Solimoea locality. They gave reasons for believing that thespecimen represents the oldest occurrence of the cebine subfam-ily in the present day Amazon basin. They noted that the speci-men is distinctly different in size and structure from any knownplatyrrhine of the Miocene to Recent. However, they resistednaming a new genus and species based on one tooth. In the inter-vening quarter-century, no further material of this peculiar mon-key has come to light and, because it was not named at that time,the specimen has received little attention. We now conclude thatthe specimen should be named and that its morphology justifiesplacing it as the sister taxon to extant Cebus. Below, we givereasons for this phylogenetic placement.
4 Lengths of m1 shearing crests are: crest 1, 1.36 mm; crest 2, 1.44 mm;
crest 3, 2.63 mm; crest 4, 1.91 mm; crest 5, 1.93 mm; crest 6, 1.41 mm. Total
crest length is 10.68 mm.
Infraorder Platyrrhini Geoffroyi, 1812Family Cebidae Bonaparte, 1831Subfamily cf. Cebinae Bonaparte, 1831
Acrecebus genus nov.
Diagnosis
With an M2 area of 74.8 mm2, (MD length 7.75 mm; BLbreadth 9.65 mm), Acrecebus has an M2 larger than the meansfor any living platyrrhine. In a sample of 92 specimens fromseven species, Alouatta M2s average 59.2 mm2 and rangefrom 37.5 to 79.8 mm2; for ten Brachyteles arachnoides spec-imens, the mean and range are 55.3 mm2 and 37.3e64.4 mm2
Shear Quotient
Solimoea acrenis
Seeds orGum
-20 -10 0 10 20
Fruit
Fruit/insects orfruit/leaves
Insects orLeaves
Fig. 7. The shearing quotient for living platyrrhine species and Solimoea bro-
ken down by dietary preference (box and whisker plot). The estimate of shear-
ing development is based on measurements of six lower molar crests (for
anatomical details, see Kay, 1975). A line with a slope¼ 1.0 was assigned
to a bivariate cluster of the natural log of m2 length (ln m2L) vs. the natural
log of the sum of the measured shearing crests (ln SH), and passing through
the mean ln m2L and mean ln SH for extant taxa. The equation expressing
this line is: ln SH¼ 1.0(ln m2L)þ 0.596. For each taxon, the expected ln
SH was calculated from this equation. The observed (measured) ln SH for
each species was compared with the expected and expressed as a residual
(shearing quotient, or SQ): SQ¼ 100� (observed� expected)/expected. Ex-
tant taxa with their dietary categories are: Callimico goeldii (insects), Brachy-
teles arachnoides (leaves), Alouatta palliata (leaves), Alouatta caraya (leaves),
Alouatta guariba (leaves), Aotus trivirgatus (fruit/leaves), Saimiri sciureus (in-
sects/fruit), Lagothrix lagotricha (fruit/leaves), Leontopithecus rosalia (fruit/
insects), Ateles geoffroyi (fruit), Callicebus moloch (fruit), Saguinus mystax
(fruit/insects), Callithrix argentata (fruit/gum), Cebuella pygmaea (gum), Pith-
ecia monachus (fruit/seeds), Cebus apella (fruit/seeds), Chiropotes satanas
(seeds/fruit), Cacajao melanocephalus (seeds/fruit). Data abstracted from
(Kay et al., 2002). Data for Solimoea come from the type lower molar.
681R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
(Kay and Frailey, 1993). Acrecebus can be further distin-guished from atelines (extant Ateles, Brachyteles, and Lago-thrix) and alouattines (extant Alouatta and MioceneStirtonia) in having a larger hypocone and a very strongly de-veloped metaconule. Unlike in any alouattine, the crown’scusps are inflated and the sides of the tooth are puffy, ratherthan straight-sided, and the occlusal surface of the crown iscorrespondingly restricted. Furthermore, unlike in alouattines,shearing crests are poorly developed; in particular, the preme-tacrista and postparacrista are short, straight, and blunt andlack a buccal cingulum or mesostyle.
In the above combination of features, Acrecebus mostclosely resembles extant Cebus. Additionally, as in Cebus,the strong metaconule is connected distally by a crest to thehypocone. The tooth differs from those of Cebus in havinga better developed lingual cingulum, a more squared crownshape, and in being three to four times larger (in a sampleof 51 specimens of Cebus capucinus, M2s average22.12 mm2 with a range of 18.67e25.19 mm2.
Acrecebus fraileyi species nov.
Etymology
From the Acre River. Named for Carl Frailey, its discoverer.
Holotype
Specimen LACM 134880 (Fig. 4C; Fig. 8), a left uppersecond molar.
Locality
Fossil vertebrate locality LACM 5158, Cachuela Bandeira,Acre River, Acre, Brazil. More geographic detail in publicationsby Frailey and colleagues (Frailey, 1987; Kay and Frailey, 1993).
Diagnosis
Diagnosis same as for genus.
Description
Kay and Frailey (1993) provided a description of thisspecimen.
Phylogenetic position of Acrecebus
As noted in the diagnosis, Acrecebus shares several inter-esting features with Cebus. Comparison of Acrecebus withall living and extinct taxa of early Miocene to Recent platyr-rhines shows that the new species shares two derived featureswith Cebus found in no other platyrrhine. First, Acrecebushas a very large metaconule. Cebus alone among platyrrhineshas a metaconule that is usually (but not always) very large.Second, in both Acrecebus and Cebus, the prehypocrista isstrongly developed and oriented buccally to reach the
metaconule. This is true also of Cebus in which the hypocone,metaconule, and metacone are aligned and joined via a lateralposterior transverse crista and a prehypocrista to form a distinctposterior crossloph, one of two that make up a ‘‘bilophodont’’condition. In Acrecebus, hypocone, metaconule, and metaconeare joined by a lateral posterior transverse crista and a prehy-pocrista, as in Cebus, although the cusps are not aligned.
A third shared-derived feature of Acrecebus and Cebus isthe inflation (bunodonty) of the molar cusps generally. Thisfeature is not a unique derived similaritydit is present alsoin some pitheciines.
Discussion
Platyrrhini today are important elements of the tropical andsubtropical faunas of South America, in some environmentsrepresented by up to 16 sympatric species. Their fossil recordis exceedingly poor, however, especially in the more equatorialregions of the continent. Middle Miocene primates of the tropicsare known only from the fauna of La Venta, Colombia, betweenw13.2 and 11.8 Ma. In the roughly ten-million-year intervalbetween the Laventan and the Pleistocene, only three specimens,all isolated and/or poorly preserved, have been identified asprimate. Thus, although meager, the new material nearly doublesthe number of specimens from this time interval.
The new and revised material described here brings to threethe number of middle Miocene primates from the Solim~oesFormation of the western Amazon region: Stirtonia sp. (previouslydescribed), Solimoea acrensis, and Acrecebus fraileyi. Stirtonia sp.is a holdover from the middle Miocene and is related to the livinghowler monkey Alouatta. Solimoea acrensis is a stem ateline andis the oldest known representative of Atelinae (wooly, spider,and muriqui monkeys). It was a large monkey, about the sizeof the living woolly monkey. It has poorly developed molarcrown crests, suggesting a diet consisting primarily of fruit.The third species, Acrecebus fraileyi, is proposed for a specimendescribed, but not named, by Kay and Frailey (1993). This
Fig. 8. A) Occlusal stereophotograph of LACM 134880, type specimen of
Acrecebus fraileyi. Mesial is to the right; buccal is to the top. Scale
bar¼ 5 mm.
682 R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
material, although scant, extends the known diversity of larger-bodied platyrrhines into the late Miocene and documents theoccurrence of a Cebus relative at this time.
In all likelihood, the real species richness of this region’s laterMiocene primate fauna must have been substantially higher thanits known richness (Kay et al., 1997). We do not have Amazo-nian representatives of many platyrrhine lineages that musthave been present somewhere on the South American continent,as evidenced either by their presence today and in the middleMiocene of Colombia (Fleagle et al., 1997) or, indirectly,from the molecular evidence of divergence times of extantclades (Barroso et al., 1997). The most likely reason for the pau-city of taxa is poor fossil samplingdsurface exposures of theSolim~oes Formation are limited and localities are rare. In thefuture, we should certainly expect to see relatives of Callicebus,pitheciins, aotines, and various callitrichines.
The apparent longevity of the taxon Stirtonia, which first ap-pears in the Colombian Miocene (Laventan) older than 13.2 Maand therefore spans at least four million years and up to sevenmillion years, is not altogether surprising since there is substan-tial (>20%) similarity between the Acre fauna and that of LaVenta, Colombia (Cozzuol, in press). However, we cautionthat the material from Acre is poorly preserved and may proveto be a different genus when better known.
The presence of a stem alouattine (Stirtonia) and a stemateline (Solimoea) confirms that these two clades had di-verged by the late Miocene and is wholly consistent witha proposed divergence time between Alouattinae and Atelinaeof between 13.6 and 14.0 Ma (Barroso et al., 1997). The pres-ence of a species related to Cebus is equally unsurprising, asmolecular evidence suggests the split time of Saimiri fromCebus at >16 Ma (Barroso et al., 1997). Indeed, what ismore surprising is the absence of a Cebus stem lineage inthe middle Miocene, particularly in the fairly well-sampledLaventan fauna.
Rosenberger and Strier (1989) reconstructed the basal ate-line as resembling the extant woolly monkey (Lagothrix) inhaving a large body size, a mixed diet of fruit and leaves (es-pecially harder fruit than in the diet of Ateles), locomotion thatwas more forelimb-dominated than in alouattines, with moreclimbing in its repertoire, and a polygynous social structure.Most elements of Rosenberger and Strier’s hypotheses cannotbe tested with the material at hand. To the extent that Solimoearesembles the hypothetical basal ateline, Rosenberger andStrier’s hypothesis regarding size is supported. However, thediet appears to have been more frugivorous like that of Atelesand less like that of Lagothrix.
Acrecebus was an exceptionally large platyrrhine monkey.Among extant platyrrhines, only atelids have evolved body sizesgreater than 4 kg. Some Pleistocene atelids may have been evenlarger than the extant ones (Cartelle and Hartwig, 1996; Hartwigand Cartelle, 1996). A second independent example of body-size increase among platyrrhines is found in the extinct pitheciidParalouatta from the island of Cuba (Horovitz and MacPhee,1999). With the cebid Acrecebus, now there is evidence thatlarge body size evolved independently in all three platyrrhinefamiliesdAtelidae, Pitheciidae, and Cebidae.
Acknowledgements
This work was supported by NSF grant BCS-0090255 toR.F. Kay and by a CNPq (Brazilian Council of Science) grantto M.A. Cozzuol. Special thanks go to Edgardo Latrubesse andthe anonymous reviewers.
Appendix I
Dental characters and character states used in the phyloge-netic analysis are described below. The number preceding eachcharacter corresponds to the one in the character-taxon matrix(Appendix II). This number is followed by a number/lettercombination that refers to the character in the published matrixof Kay et al. (2004). Characters followed by an asterisk areconsidered ordered in the phylogenetic analysis. Details aboutthe source of the characters are provided by Kay et al. (2004).Tooth areas are calculated as the product of mesiodistal lengthand buccolingual breadth. In some cases, the character impliesthat both m1 and m2 are needed whereas we have just one toothfor our fossil. The character is so worded because we find nodifference between the morphology of m1 and m2 in any livingtaxon, and we assume this also to be the case in the fossil.
Characters that rely upon linear measurements are based onthe samples documented in Plavcan (1990). In total, the sampleincludes 290 individual specimens of atelids as follows:Alouatta seniculus group (includes A. seniculus, A. belzebul,A. guariba, A. macconnelli), 121; Alouatta caraya group(includes A. caraya, A palliata, and A. pigra), 92; Lagothrixlagotricha (includes L. lagotricha, L. cana, and L. poeppigii),23; Ateles geoffroyi, 44; Brachyteles arachnoides, 10. Seventy-six specimens were evaluated for the discrete character data asfollows: Alouatta seniculus group (includes A. seniculus, A.belzebul, A. guariba, and A. macconnelli), 15; Alouatta carayagroup (includes A. caraya, A palliata, and A. pigra), 7; Lagothrixlagotricha (includes L. lagotricha, L. cana, and L. poeppigii), 23;Ateles geoffroyi, 17; Brachyteles arachnoides, 14.
Material comes from the following collections: Academyof Natural Sciences, Philadelphia, PA, USA; The NaturalHistory Museum, London, England, UK; Field Museum ofNatural History, Chicago, IL, USA; National Museum ofNatural History (Smithsonian Institution), Washington, DC,USA; Museu de Zoologia da Universidade de Sao Paulo, Brazil.
Lower molars
1. m2. m1 root number: 0¼ one; 1¼ two.2. m3. m2 root number: 0¼ one; 1¼ two.3. m6*. m2 trigonid width (ratio of buccolingual breadths of
trigonid and talonid): 0¼much wider than talonid(�1.11); 1¼widths similar (<1.11, >0.90); 2¼muchnarrower than talonid (�0.90).
4. m8*. m1 paraconid position: 0¼mesial to protoconid;1¼mesiolingual, between protoconid and metaconid;2¼mesial to metaconid but widely spaced from it;3¼ twinned with metaconid.
683R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
5. m9*. m2 paraconid position: 0¼mesial to protoconid;1¼mesiolingual, between protoconid and metaconid;2¼mesial to metaconid but widely spaced from it;3¼ twinned with metaconid.
6. m11. m1 parastylid: 0¼ absent; 1¼ present.7. m12*. Molar metastylids: 0¼ absent; 1¼ small; 2¼ large.8. m15*. Molar enamel surface: 0¼ smooth; 1¼ slightly
crenulated; 2¼ highly crenulated.9. m16*. m1 trigonid height (ratio of trigonid height to talonid
height measured on the buccal aspect of the crown): 0¼ higherthan talonid (�1.20); 1¼ slightly higher than talonid (�1.10,<1.20); 2¼ trigonid and talonid of similar height (<1.10).
10. m17. m1e2 cusp relief: 0¼moderate to high; 1¼ low.11. m18. m1 trigonid lingual configuration: 0¼ open;
1¼ closed.12. m19. m1 metaconid position: 0¼ transversely aligned, lin-
gual to protoconid; 1¼ slightly distolingual to protoconid.13. m20*. m1e2 paraconid development: 0¼ absent; 1¼ small;
2¼ large.14. m21. m1e2 lateral protocristid orientation: 0¼ runs
toward metaconid; 1¼ runs toward hypoflexid.15. m22. m1 distal trigonid wall: 0¼ complete; 1¼ deeply
notched by protoconid/metaconid sulcus; 2¼medial andlateral protocristid do not meet, but no sulcus is visible.
16. m23. m2 distal trigonid wall: 0¼ complete; 1¼ deeplynotched by protoconid/metaconid sulcus; 2¼medialand lateral protocristid do not meet but no sulcus is visible.
17. m24. m1e2 wear facet X: 0¼ present; 1¼ absent.18. m25*. m1e2 entoconid: 0¼ absent; 1¼ barely stands out
on lingual talonid marginal crest; 2¼ a small discretecusp; 3¼ a large cusp.
19. m26*. m1e2 postentoconid sulcus: 0¼ prominent; 1¼ faintlyvisible; 2¼ absent.
20. m27*. m1 hypoconulid size: 0¼ large; 1¼moderate;2¼ small; 3¼ absent.
21. m28*. m2 hypoconulid size: 0¼ large; 1¼moderate;2¼ small; 3¼ absent.
22. m30*. m1e2 hypoconulid position: 0¼ twinned to ento-conid; 1¼ near midline; 2¼ slightly buccal to midline.
23. m31*. m1e2 cristid obliqua development: 0¼weak(rounded); 1¼ strong (trenchant); 2¼ very strong (trenchant).
24. m32*. m1 cristid obliqua orientation: 0¼ reaches trigonidwall at a point distal to protoconid; 1¼ reaches trigonidwall at a point distolingual to protoconid; 2¼ reachestrigonid wall at a point distal to metaconid.
25. m33*. m2 cristid obliqua orientation: 0¼ reaches trigonidwall at a point distal to protoconid; 1¼ reaches trigonidwall at a point distolingual to protoconid; 2¼ reachestrigonid wall at a point distal to metaconid.
26. m34. m1 cristid obliqua terminus: 0¼ runs to base oftrigonid; 1¼ runs part way up the distal trigonid wall;2¼ connects with protoconid tip or protocristid;3¼ connects with metaconid.
27. m35. m2 cristid obliqua terminus: 0¼ runs to base oftrigonid; 1¼ runs part way up the distal trigonid wall;2¼ connects with protoconid tip or protocristid;3¼ connects with metaconid.
28. m37.m1e2centroconiddevelopment:0¼ present;1¼ absent,but cristid obliqua bends sharply in hypoflexid; 2¼ absent.
29. m38*. m1e2 hypocristid development: 0¼ absent or seenonly as a trace; 1¼weak; 2¼ strong.
30. m40*. Lingual configuration of m1e2 talonid: 0¼ open;1¼ notched lingually but not open; 2¼ closed.
31. m41. m1e2 distal fovea: 0¼ absent; 1¼ present.32. m42. m1e2 hypocristid configuration: 0¼ simple;
1¼with accessory cusp close to hypoconid.33. m43. m1e2 cristid obliqua: 0¼ notched; 1¼ straight.34. m44*. Molar cusp inflation: 0¼ cusps not inflated, mar-
ginally positioned; 1¼ slightly inflated; 2¼ very inflated.35. m45*. m1e2 buccal cingulum development: 0¼ absent to
trace; 1¼ partial, broken at protoconid and hypoconid;2¼ complete.
36. m46*. m1 hypoflexid depth: 0¼ very shallow;1¼moderate; 2¼ deep.
37. m47*. m2 hypoflexid depth: 0¼ very shallow;1¼moderate; 2¼ deep.
38. m54*. m1 area: 0¼ 1.10e2.10 mm; 1¼ 2.10e3.10 mm;2¼ 3.10e4.10 mm; 3¼ 4.10e5.10; 4¼ 5.10e6.10 mm;5¼ 6.10e7.10 mm; 6¼ 7.10e8.10 mm; 7¼ 8.10e9.10 mm; 8¼>9.10.
39. m55*. m1 mesiodistal length/buccolingual breadth:0¼ 1.0e1.15; 1¼ 1.16e1.22; 2¼ 1.23e1.32; 3¼>1.33.
40. m56. Convergence of buccal and lingual molar cusp walls:0¼ convergent; 1¼ vertically sided.
41. m57. m1e2 entoconid position relative to hypoconid:0¼ transverse to hypoconid; 1¼ distal to hypoconid.
Upper premolars
42. P2*. P3 root number: 0¼ one; 1¼ two; 2¼ three.43. P3*. P4 root number: 0¼ one; 1¼ two; 2¼ three.44. P7. P4 occlusal outline: 0¼ triangular; 1¼ suboval;
2¼ squared.45. P8. P3e4 trigon/talon proportions: 0¼ trigon� talon;
1¼ trigon< talon.46. P9. P3 protocone: 0¼ present; 1¼ absent.47. P10. P4 metacone: 0¼ absent; 1¼ present.48. P11. P4 protocone: 0¼ low relative to paracone; 1¼ high
relative to paracone.49. P13. Premolar hypocones: 0¼ absent; 1¼ present on P4
only; 2¼ present on P3e4; 3¼ present on P2e4.50. P14*. P4 paraconule: 0¼ large; 1¼ small; 2¼ absent.51. P15. P3e4 parastyles: 0¼ present; 1¼ absent.52. P16. P3e4 metastyles: 0¼ absent; 1¼ present.53. P17. P3e4 postprotocrista: 0¼ strong; 1¼weak, short.54. P18. P3 distal crown margin: 0¼ straight or smoothly
convex; 1¼waisted between buccal and lingual cusps.55. P19. P3e4 lingual cingulum: 0¼ absent or weak;
1¼ strong.56. P20. P3 metacone: 0¼ absent; 1¼ present.57. P21. P3e4 buccal cingulum development: 0¼ absent or
weak; 1¼ strong.
684 R.F. Kay, M.A. Cozzuol / Journal of Human Evolution 50 (2006) 673e686
Ap
pen
dix
II
Cha
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Alo
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90
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Alo
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11
29
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01
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19
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1
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