STATUS OF PROECHIMYS ROBERTI AND P. ORIS (RODENTIA: ECHIMYIDAE) FROM EASTERN AMAZONIA AND CENTRAL...

109

Journal of Mammalogy, 82(1):109–122, 2001

STATUS OF PROECHIMYS ROBERTI AND P. ORIS(RODENTIA: ECHIMYIDAE) FROM EASTERN AMAZONIA

AND CENTRAL BRAZIL

MARCELO WEKSLER,* CIBELE R. BONVICINO, IVONE B. OTAZU, AND JOSE S. SILVA JUNIOR

Laboratorio de Vertebrados, Universidade Federal do Rio de Janeiro,Rio de Janeiro, Brazil (MW, JSS)

Genetics Section, Instituto Nacional de Cancer, 20230-130, Rio de Janeiro, Brazil (CRB, IO)Present address of MW: Department of Mammalogy, American Museum of Natural History,

Central Park West at 79th Street, New York, NY 10024-5192

Proechimys roberti has been considered an isolate representative of the guyannensis groupof species of the genus Proechimys in the Cerrado of central Brazil, or regarded as amember of the longicaudatus group of species. We present new karyologic, morphometric,morphologic, and molecular data from populations spanning the gap between the previouslyknown isolated distribution of P. roberti and the core distribution of the guyannensis group.All specimens had the same basic karyotype, 2n 5 30, with fundamental number (FN) 554–55. FN variation was due to a pericentric inversion affecting a small autosomal pair.Specimens from the eastern Amazon Basin and the Cerrado did not have any differentiationin external, cranial, and dental characters. In contrast, samples showed a significant mul-tivariate morphometric variation, with a high heterogeneity among all populations, inde-pendent of Cerrado or Amazon location. Our results, coupled with phylogenetic analysisof cytochrome-b sequences, indicate that P. roberti is a valid species of the guyannensisgroup and that the species of this group occurring in eastern Amazon, P. oris, is probablya junior synonym of P. roberti.

Key words: Brazil, cytochrome-b, cytogenetics, Echimyidae, morphometrics, Proechimys oris,Proechimys roberti, Rodentia, taxonomy

Because of difficulties in identifying dis-crete morphologic characters of Proechi-mys, controversial taxonomic arrangementsand disparate criteria for defining its sub-ordinated taxa have been proposed. As stat-ed by Thomas (1928), these rodents arecharacterized by extensive morphologicvariability, with overlapping morphologiccharacters between species. A recent check-list (Woods 1993) attributed 27 species tothe genus (herein considered as comprisingonly the former subgenus Proechimys, giv-en the evidence of nonmonophyletism ofProechimys and Trinomys—Lara et al.1996), although other authors recognized 8

* Correspondent: [email protected]

or 4 species (Cabrera 1961; Moojen 1948),with several subspecies. Patton (1987) rec-ognized 9 species groups of Proechimysbased on morphologic criteria: guyannensis,goeldii, longicaudatus, simonsi, cuvieri,trinitatus, semispinosus, canicollis, and de-cumanus.

Karyologic data potentially can be usefulfor the identification of Proechimys taxa.Species of the genus show considerablevariation in diploid chromosome number(2n), ranging from 2n 5 14 to 2n 5 62,with roughly 45 karyotypes described todate (Aguilera and Corti 1994; Aniskin1994; Barros 1978; Bueno and Gomez-Lav-erde 1993; Bueno et al. 1989; da Silva

110 Vol. 82, No. 1JOURNAL OF MAMMALOGY

1998; Gardner and Emmons 1984; Georgeand Weir 1973; Gomez-Laverde et al. 1990;Leal-Mesquita 1991; Maia and Langguth1993; Patton and Gardner 1972; Reig 1989;Reig and Useche 1976; Reig et al. 1979).Such variation prompted some authors(Aguilera and Corti 1994; Reig and Useche1976) to hypothesize that karyotypic diver-gence was profoundly relevant to speciationin Proechimys.

One of the species with a convoluted tax-onomic history is Proechimys robertiThomas, 1901, with type locality in the RioJordao, Araguari, State of Minas Gerais,Brazil. In his original description, Thomas(1901) considered P. roberti to be closelyrelated to P. longicaudatus, and some sub-sequent reports treated roberti as a subspe-cies of P. longicaudatus (Cabrera 1961;Moojen 1948). Thomas (1904) modified hisoriginal statement and indicated that P. ro-berti was related to P. cayennensis (5 P.guyannensis), leading Ellerman (1940) topropose that roberti was a subspecies of P.cayennensis. Finally, Patton’s (1987) mor-phologic analysis placed P. roberti as anisolate member of the guyannensis group inthe states of Goias and Minas Gerais in cen-tral Brazil. However, the last checklist ofthe genus still treated roberti as a juniorsynonym of P. longicaudatus (Woods1993).

The name attributed to the form of theguyannensis group found in the easternAmazon is P. oris Thomas, 1904 (Cabrera1961; Woods 1993), with type locality Iga-rape-Assu, near Belem, state of Para, Bra-zil. In contrast to P. roberti, P. oris alwayshas been tied to P. guyannensis, regardedeither as a subspecies (Cabrera 1961; Moo-jen 1948), or as a valid species within theguyannensis group (Patton 1987; Woods1993).

Pessoa et al. (1990) presented a morpho-metric study of 4 populations of the guy-annensis group from the Amazon Basin andnortheastern and central Brazil, includingsamples regarded as P. roberti and P. oris.The authors concluded that the high level

of morphometric differentiation foundcould be regarded as evidence of distinctevolutionary units for the populations; inthis context, Pessoa et al. (1990) claimed aclassification that reflected this distinctive-ness.

We present new data on Proechimys fromthe eastern Amazon Basin and the Cerradoof central Brazil. Specimens that we ana-lyzed agree with morphologic characteriza-tion of the guyannensis group given by Pat-ton (1987), by possessing the set of mor-phologic traits that distinguish it from theother possibly sympatric Proechimysgroups (e.g., longicaudatus, goeldii, cuvi-eri). Our data fill the gap between the pre-viously known distribution of P. robertiand the core of the distribution of the guy-annensis species group in the Amazon Ba-sin, presenting 5 new localities and samplesfrom localities formerly referred to as mem-bers of the guyannensis species group. Weanalyzed the degree of karyotypic, morpho-logic, morphometric, and molecular diver-gence among populations and examined thepresent taxonomic arrangement of P. ro-berti and P. oris.

MATERIALS AND METHODS

Karyotypic, morphometric, morphologic, andmolecular data were collected from 162 speci-mens of Proechimys from 24 localities in Brazil,Venezuela, and Guyana. Specimens were depos-ited in museums or referred to by field numbersaccording to the following acronyms: MuseuNacional, Rio de Janeiro (MN); Museu ParaenseEmılio Goeldi, Belem (MPEG); American Mu-seum of Natural History, New York (AMNH);United States National Museum, Washington,D.C. (USNM); Instituto de Pesquisa da Ama-zonia, Manaus (INPA); Royal Ontario Museum,Toronto (ROM); Laboratorio de Vertebrados,Universidade Federal do Rio de Janeiro, Rio deJaneiro (LV); C. R. Bonvicino (CRB); J. L. Pat-ton (JLP); M. N. F. da Silva (MNFS); A. L.Gardner (ALG); CM, DSR, and CS refer tospecimens deposited in the INPA collection.

Site localities 1–24 (Fig. 1) were as follows.1) Brazil, Para, Curua-Una (28249S, 548059W),in the Amazonian region. Ten specimens were

WEKSLER ET AL.—STATUS OF PROECHIMYS ROBERTIFebruary 2001 111

FIG. 1.—Localities of specimens: 1) Curua-Una, 2) Primavera, 3) Patagonia, 4) Capim, 5) Cameta,6) Fazenda Lagoa Nova, 7) Fazenda Osara II, 8) Serra do Lajeado, 9) Fazenda Fiandeira, 10) Ana-polis, 11) Faro, 12) Limao, 13) Churi Tepui, 14) Auyan-Tepui, 15) Rio Xingu, 16) Maraba, 17)Niquelandia, 18) PDBFF, 19) Colocacao Bigorna, 20) Rio Tiquie, 21) Rio Mawarinuma, 22) AltoJatapu, 23) Paujı, and 24) Loo Creek. Circles with a dot in the center designate type localities ofProechimys oris (A, Igarape-Assu, Para, Brazil) and P. roberti (B, Rio Jordao, Minas Gerais, Brazil).Specimens from localities 1, 3, 4, and 9–14 were used in morphometric analysis; specimens fromlocalities 2 and 6–9 were karyotyped; and specimens from localities 9 and 15–24 were used inmolecular analysis (Fig. 5). The circle around localities 9 and B is an approximation of the distributionof P. roberti given by Moojen (1948) and Patton (1987). The shaded area indicates the approximatedistribution of Amazonian moist broadleaf forest.

included in morphometric analysis (malesMPEG 9061, 9062, 9064, 9067, 9069, 9072,15390, 15391, 15392, 15394). Gardner and Em-mons (1984) identified 1 karyotyped specimenfrom this locality as P. oris, after comparisonwith the holotype of this species. 2) Brazil, Para,Primavera (18209S, 488349W), in the Amazonianregion. Two specimens (females CRB 604 and606) were livetrapped in the ‘‘terra firme’’ for-est. One specimen (604) was karyotyped; nonewas included in morphometric analysis. Skinsand skulls were deposited in the mammal col-lection of MN. 3) Brazil, Para, Patagonia

(18179S, 478589W), in the Amazonian region.Nine specimens were included in morphometricand morphologic analyses (females AMNH75143, 75144, 75147, 75151; males AMNH75146, 75152, 75155, 75156; AMNH 75150,sex unknown). 4) Brazil, Para, Capim (18419S,478449W), in the Amazonian region. Three spec-imens were included in morphometric and mor-phologic analysis and pooled with specimensfrom Patagonia (female AMNH 188972; malesAMNH 203442, 203493). 5) Brazil, Para, Baiao,Ilha do Taiuna and Cameta (28159S, 498299W),3 adjacent localities in Rio Tocantins, in the Am-


azonian region. Three specimens were analyzedmorphologically but not included in morpho-metric analysis (females AMNH 37484, 96817;male AMNH 96898). 6) Brazil, Maranhao, Fa-zenda Lagoa Nova, about 32 km NW of Baca-bal, along road BR-316 (48049S, 448589W), a lo-cality in the Amazonian part of the ‘‘Zona dosCocais.’’ Two specimens (female MPEG 29000;male MPEG 29001) were collected with livetraps in Orbignya palm fields (known locally as‘‘Babacual’’) associated with secondary Ama-zonian forest. One specimen (MPEG 29000)was karyotyped; none was included in morpho-metric analysis. 7) Brazil, Tocantins, FazendaOsara II, Sao Sebastiao (58179S, 488189W), inthe ecotone between Amazonian forest and Cer-rado. Three specimens (females LV-FO 24, 28,and male LV-FO 17) were livetrapped in re-maining forest vegetation along riverbanks. All3 specimens were karyotyped; none was includ-ed in morphometric analysis. Skins and skullswere deposited in the mammal collection ofMN. 8) Brazil, Tocantins, Serra do Lajeado, La-jeado (98539S, 488179W), in the Cerrado biome.Two specimens were collected with live traps ingallery forest (female LV-LJ 28; male LV-LJ 15)and were karyotyped but not included in mor-phometric analysis. Skins and skulls were de-posited in the mammal collection of MN. 9)Brazil, Goias, Fazenda Fiandeira, 65 km SSWof Cavalcante (148049S, 478459W), in the Cer-rado Biome. At that locality, 32 specimens werelivetrapped in the following habitats: 27 in gal-lery forest, 3 in ‘‘cerradao,’’ and 2 in ‘‘cerradosensu stricto’’ bordering gallery forest. All adultspecimens were measured and 18 were karyo-typed (indicated with *): females MN 50193,50194, 50195*, 50197*, 50198*, 50199,50200*, 50201*, 50202*, 50203*, 50204*,50205, 50206*, 50207*, 50209, 50213*, 50216,50218, 50219, 50220, 50221 and males MN50193, 50196, 50208*, 50210*, 50211*, 50212,50214*, 50215*, 50217*, 50222, 50223*. Twospecimens were included in molecular analysis:MN 50219, 50221. 10) Brazil, Goias, Anapolis(168209S, 488589W), in the Cerrado biome. Four-teen specimens were included in morphometricanalysis (females MN 4032, 4034, 4042, 4048,4054, 4064, 34159, 34160; males MN 4033,4037, 4045, 4046, 4078; MN 4036, sex un-known). Patton (1987) identified specimensfrom that locality as P. roberti. 11) Brazil, Para,north bank of Rio Amazonas, Rio Nhamunda,

Faro (28119S, 568449W), in the Amazonian re-gion. Seventeen specimens were used in mor-phometric analysis (females AMNH 93987,93988, 93989, 93990, 93992, 93998, 94000,94004, 94007, 94008, 94015, 94018, 94187;males AMNH 94009, 94012, 94013, 94017). 12)Brazil, Roraima, Rio Cotinga, Limao (38569N,608309W), in savannas of the Guyanan region.Eighteen specimens were included in morpho-metric analysis (females AMNH 75419, 75422,75427, 75429, 75438, 75440, 75460; malesAMNH 75418, 75423, 75424, 75426, 75432,75434, 75443, 75446, 75465, 75474, 75481).13) Venezuela, Bolivar, Churi Tepui (58139N,618549W), in the ecotone between Pantepuis andsavannas of the Guyanan region. Two specimenswere pooled with specimens from Auyan-Tepuiand included in morphometric analysis (maleAMNH 176341; AMNH 176343, sex unknown).14) Venezuela, Bolivar, Auyan-Tepui (58459N,628309W), in the Pantepuis biome. Twenty-fivespecimens were included in morphometric anal-ysis (females AMNH 130740, 130741, 130742,130747, 130751, 130752, 130753, 130754,130759, 130766, 130768, 130772, 130776,130786; males AMNH 130735, 130737,130738, 130748, 130749, 130750, 130756,130760, 130761, 130769, 130788). 15) Brazil,Para, right bank Rio Xingu, 52 km SSW Alta-mira (38399S, 528229W), in the Amazonian re-gion. Three specimens were included in molec-ular analysis (USNM 549582, 549586, 549587).16) Brazil, Para, Maraba, Floresta Nacional Ta-pirape–Aquirı (58489050S, 508309540N), in theAmazonian region. Three specimens were in-cluded in molecular analysis (CS 14, 21, 25).17) Brazil, Goias, Niquelandia (148279S,488279W), in the Cerrado biome. One specimenwas included in molecular analysis (DSR 3758).18) Brazil, Amazonas, 80 km N Manaus,PDBFF (28239S, 598519W), in the north bank ofthe Amazonas River. One specimen was includ-ed in molecular analysis (CM 42). 19) Brazil,Amazonas, Rio Araca, Igarape Limao, Coloca-cao Bigorna (about 08159S, 638109W), in thenorth bank of the Amazonas River. One speci-men was included in molecular analysis (MNFS1796). 20) Brazil, Amazonas, Sao Gabriel daCachoeira, right bank Rio Tiquie (about 08089S,678059W), in the north bank of the AmazonasRiver. Two specimens were included in molec-ular analysis (INPA 2533, 2534). 21) Venezuela,Amazonas, Rio Mawarinuma (ca. 18119N,


668259W) in the Amazonian region. Four spec-imens were included in the molecular analysis(ALG 14242, 14255, 14283, 14297). 22) Brazil,Roraima, Sao Joao da Baliza, UHE Alto Jatapu(about 08579010N, 598549400W), in the northbank of the Amazonas River. Three specimenswere included in molecular analysis (MN 42831,61642, 61643). 23) Venezuela, Bolivar, 4 km SE(by road) Paujı (about 48239N, 618409W), in theGuyanan Highland moist forest ecoregion. Onespecimen was included in molecular analysis(JLP 9044). 24) Guyana, Demerara–Mahaica,Loo Creek, 68 km S (by road) Georgetown(68149N, 588159W), in the Guyanan moist forestecoregion. One specimen was included in mo-lecular analysis (ROM 98216).

Chromosome preparations were obtainedfrom bone marrow cultures in RPMI 1640 me-dium, 20% fetal calf serum, ethidium bromide(5 mg/ml), and colchicine 1026 M for 2 h, orfrom primary cultures of kidney epithelium inDulbecco minimal essential medium with 10%fetal calf serum after 5 h of treatment with col-chicine with the addition of ethidium bromidefor the last 2 h. C- and G-banding followedSumner (1972) and Seabright (1971), respec-tively.

For morphometric comparisons, we took 15craniodental measurements (Bonvicino andWeksler 1998): greatest skull length, condylo-incisive length, breadth across occipital con-dyles, length of diastema, length of palatalbridge, length of maxillary tooth row, length ofincisive foramen, breadth of incisive foramen,rostral length, rostral breadth, least interorbitalbreadth, orbital length, zygomatic breadth,breadth of braincase, and cranial height. Cranialand dental measurements were taken with digitalcalipers.

Only animals with all molar teeth erupted andfunctional (notably worn teeth) were included inmorphometric analysis. The analysis was aimedto detect differences in the multivariate spacebetween populations, as described by Pessoa etal. (1990). Following Bookstein (1989), weavoid referring to ‘‘size and shape’’ in our anal-ysis, although the method herein employed canbe considered to be similar to the ‘‘size-inde-pendent’’ canonical discriminant analysis de-scribed by Reis et al. (1990). Based on the Bur-naby correction method, the 1st eigenvector ofthe principal component analysis obtained fromthe pooled within covariance matrix of logarith-

mic variables was set apart from the rest of theeigenvectors (Burnaby 1966; Rohlf and Book-stein 1987). The 1st principal component wascompared using analysis of variance, with Tukeytest for contrasting means. Scores of the remain-ing principal components (14) were calculatedand analyzed by a canonical discriminant anal-ysis. All statistical analyses were performedwith the SAS version 6.12 (PROC GLM, PROCCANDISC, and PROC PRINCOMP—SAS In-stitute Inc. 1996).

Our morphologic analysis was restricted toexternal and cranial characters. To assess varia-tion of characters deemed as pivotal by Moojen(1948), Patton (1987), and Thomas (1904), wefocused on the overall external pelage and thecounterfold pattern of the molar teeth.

Molecular data were collected by J. L. Pattonand M. N. F. da Silva, who kindly provided thedata for analysis. Sequences of the first 372 ba-ses of mitochondrial cytochrome-b (81 parsi-mony-informative characters) were analyzed.Maximum parsimony cladograms were con-structed using the branch and bound search op-tion of PAUP* (version 4.0b2a—Swofford1999). Bootstrap analysis (Felsenstein 1985),with 100 replicates using heuristic search with10 random additions each, was performed toevaluate the support of nodes in the phylogeny.Pairwise sequence divergence was calculated asKimura 2-parameter distance (Swofford et al.1996).

RESULTS AND DISCUSSION

Karyotypic variation.—Karyotypic anal-ysis of all 25 Proechimys specimensshowed that 2n 5 30 and fundamental num-ber (FN) 5 54–55. The autosomal comple-ment was composed of 13 pairs of biarmedchromosomes and 1 small pair of acrocen-trics. The X chromosome was a large sub-metacentric, and the Y chromosome was asmall acrocentric (Fig. 2). With convention-al Giemsa staining, both members of pair 9showed a secondary constriction at the longarm. Variation in fundamental number,found in the Fazenda Fiandeira and Pri-mavera populations, was due to a pericen-tric inversion in 1 member of the small ac-rocentric pair. C-banding revealed smallamounts of heterochromatin in 7 autosome


FIG. 2.—Nondifferentially stained (female MN 50203) and G-banded (male MN 50217) karyotypeof Proechimys roberti.

FIG. 3.—C-banded karyotype of Proechimysroberti (male MN 50217); arrows indicate the Xand Y chromosomes.

pairs, mainly at centromeric regions butalso in telomeric regions. In the X chro-mosomes, constitutive heterochromatin waspresent at telomeres, the pericentromeric re-gion, and an interstitial region in the middleof the long arm (Fig. 3).

The karyotype described herein is thesame as that reported by Svartman (1989)in specimens from Brasılia (Distrito Fed-eral) and differed by a single pericentric in-version from those attributed to P. oris (2n5 30, FN 5 56) by Gardner and Emmons(1984) and Leal-Mesquita (1991), althoughReig et al. (1980) attributed a different kar-yotype (2n 5 30, FN 5 52) to this species.In view of this conflicting data, we consid-ered the 2n 5 30, FN 5 56 karyotype asvalid for P. oris based on the fact that the


animal karyotyped by Gardner and Em-mons (1984) was compared with the P. orisholotype. We also found a karyotype simi-lar to the 1 found by Gardner and Emmons(1984) and Leal-Mesquita (1991) in a spec-imen from a locality (Primavera) 110 kmfrom the type locality of P. oris (Igarape-Assu). Other species of the guyannensisgroup were found to share a similar fun-damental number (Table 1) despite showingdifferent diploid numbers (varying from 30to 40), probably as a result of centric fu-sions.

Specimens collected in the Cerrado andAmazonian regions were karyologicallyidentical. Moreover, the fact that popula-tions (Cavalcante and Primavera) showedthe same variation in fundamental number(54–55) suggested that the pericentric in-version might be maintained as a chromo-some polymorphism and individuals with2n 5 30, FN 5 56 are expected to be found.

In contrast, additional species of Proe-chimys also share the same diploid numberof P. roberti (2n 5 30; Table 1), althoughdiffering in fundamental number and chro-mosome morphology. The karyotype re-ported herein is similar in diploid and fun-damental number to those of P. semispi-nosus of Costa Rica (Patton and Gardner1972) and P. decumanus of Ecuador (Gard-ner and Emmons 1984). However, the kar-yotype of P. roberti is different from thosespecies because of the larger size of auto-somal pairs 2 and 3 and presence of a biar-med X chromosome, which is acrocentricin P. semispinosus and P. decumanus. Thekaryotype described here (2n 5 30, FN 554–55) differed in diploid number, funda-mental number, and chromosome morphol-ogy from the karyotype of the species oflongicaudatus group (Table 1), providingevidence against the inclusion of P. robertiwithin this group.

Morphometric variation.—Descriptivestatistics of the 7 samples totaling 121 spec-imens are shown in Table 2. Results of mul-tivariate morphometric analysis showedthat the 1st eigenvector of the principal

component analysis contained highly het-erogeneous coefficients, although all vari-ables showed positive loadings, from 0.060(length of maxillary tooth row) to 0.391(breadth of incisive foramen). The postu-lation that the 1st eigenvector representedan isometric-size component required thatall coefficients were equal to 0.258 (the in-verse of the square root of the number ofvariables—Jolicoeur 1963). However, fewvariables (greatest skull length, condylo-in-cisive length, length of palatal bridge, ros-tral breadth, zygomatic breadth) showed co-efficients close to that value, indicating ahigh degree of allometric influence in the1st component. This size-related factor pre-sented a significant difference between pop-ulations (F 5 11.29, d.f. 5 6, 109, P ,0.0001). The localities Limao and Faro dif-fered from all others in contrast betweenmeans, but the other samples did not showsignificant differences.

Canonical discriminant analysis of the re-maining principal components indicated 6functions differentiating all populations.The squared Mahalanobis distance betweenpairs of populations varied from 7.66 (Li-mao and Auyan-Tepui) to 32.02 (FazendaFiandeira and Faro); all distances were sig-nificant (P , 0.0001). The plot of the first2 canonical functions (Fig. 4) showed thatalthough all populations presented statisti-cally significant differences, this could notbe ascribed to a simple pattern of 1 function(plots of the remaining functions followedthe same general pattern in Fig. 4). The first2 canonical functions, which accounted for61.9% of the remaining variance, differen-tiated the Faro and Limao populations fromthe others. A slight separation also existedof samples from Fazenda Fiandeira and An-apolis from Auyan-Tepui, Patagonia, andCurua-Una. Only the projection of all ca-nonical function scores in 6-dimensionalhyperspace completely separated all popu-lations.

Both the 1st principal component fromthe pooled-within matrix and the canonicalfunctions from the remaining components


TABLE 1.—Karyotypes of Proechimys; names in parentheses are as in references.

Groupa

Species 2n FN Locality Referenceb

guyannensis

P. oris 30 56 Curua-Una, Para, Brazil 7, 10P. roberti 30 54–55 Goias, Tocantins, and Maranhao, Bra-

zilThis report

P. cherriei 40 54 Cairara del Orinoco, Venezuela 14P. guyannensis 40 54 Cayenne and Saul, French Guiana 15P. cf. pattoni (guyan-

nensis)40 56 Balta, Loreto, Peru 12

P. pattoni 40 56 Rio Jurua, Amazonas, Brazil 6P. gardneri 40 56 Rio Jurua, Amazonas, Brazil 6

goeldii

P. steerei 24 42 Pucallpa, Peru; Loreto, Peru; southernPeru

7, 12, 14

P. cf. steerei 24 44 Ucayali, Peru 2P. amphichoricus 26 44 Territorio Federal Amazonas, Vene-

zuela14

P. quadruplicatus 28 44 Limoncocha, Napo, Ecuador 7P. quadruplicatus 28 42 La Poza, Santiago, Peru 7

longicaudatus

P. longicaudatus 28 48 Rio Jamari, Roraima, Brazil 10P. brevicauda 28–30 48–50 Southern Peru 7P. gularis 30 48 Limoncocha, Ecuador 7Proechimys sp. 1 28 51–52 Ucayali, Peru 2Proechimys sp. 2 30 50 Ucayali and Loreto, Peru 2Proechimys sp. 3 28 51–52 Loreto, Peru 2Proechimys sp. 4 34 56 Loreto, Peru 2

simonsi

P. simonsi (hendeei) 32 58 Balta, Peru; Putumayo, Colombia 12, 14P. simonsi 32 58 Ecuador and southern Peru 7P. cf. simonsi 32 57–58 Ucayali and Loreto, Peru 2

cuvieri

P. cuvieri 28 46 Rio Uatuma, Amazonas, Brazil 11P. cuvieri 28 50 Cayenne, French Guyana 15

trinitatis

P. poliopus 42 72 Tachira, Zulia, and Merida, Venezue-la

14

P. poliopus 42 76 Kasmera, Los Angeles del Tucuco,Venezuela

1

P. guairae 44–50 72 Aragua, Venezuela 13P. guairae 46–52 72–74 El Limon, Turiamo, Palmero, Turen,

Cueva de Agua and San Juan deAreo, Venezuela

1

P. guairae 46 68 Aragua, Carabobo, and Falcon, Vene-zuela

14

P. guairae 46 70 Ocumare, Aragua, Venezuela 8P. mincae 48 68 Minca (topotypes), Magdalena, Co-

lombia7

P. guairae spp. 50 66 Cojedes and Portuguesa, Venezuela 14P. trinitatis 62 80 Cueva del Guacharo, Venezuela 1P. trinitatis (P. urichi) 62 76 Monagas, Venezuela 14


TABLE 1.—Continued.

Groupa

Species 2n FN Locality Referenceb

P. urichi (Proechimyssp.)

62 66 Barinas, Venezuela 14

Proechimys sp. semi-spinosus

62 74 Guaquitas, Tierra Buena Las Matas,and La Nulita, Venezuela

1

P. semispinosus 30 50 Isla Gorgona, Colombia; Choco, Co-lombia

4, 9

P. semispinosus 30 52 Santa Rosa, Ecuador 7

rosa

P. semispinosus 30 50–54 Limon, Costa Rica; Canal Zone, Pan-ama; Valle, Colombia; Esmeraldasand El Oro, Ecuador

7, 12

P. oconnelli 32 52 Meta, Colombia 7

canicollis

P. canicollis 24 44 Bonda (topotypes), Magdalena, Co-lombia; Rio Cachiri, Venezuela

1, 7

decumanus

P. decumanus 30 54 Aguas Verdes (topotypes), Tumbes,Peru and Guayas and El Oro, Ec-uador

7

Unknown

P. echinothrix 32 60 Rio Jurua, Amazonas, Brazil 6P. kulinae 34 52 Rio Jurua, Amazonas, Brazil 6Proechimys sp. 5 14–16 18 Amazonas, Brazil 3Proechimys sp. 6 30 52 Rio Jamari, Roraima, Brazil 10Proechimys sp. 7 32 54 Boyaca, Colombia 5Proechimys sp. 8 44 52 Manaus, Amazonas, Brazil 10

a Species grouped according to Patton (1987).b 1 5 Aguilera and Corti (1994), 2 5 Aniskin (1994), 3 5 Barros (1978), 4 5 Bueno and Gomez-Laverde (1993), 5 5 Bueno

et al. (1989), 6 5 da Silva (1998), 7 5 Gardner and Emmons (1984), 8 5 George and Weir (1973), 9 5 Gomez-Laverde et al.(1990), 10 5 Leal-Mesquita (1991), 11 5 Maia and Langguth (1993), 12 5 Patton and Gardner (1972), 13 5 Reig (1989), 14 5Reig and Useche (1976), 15 5 Reig et al. (1979).

showed differences between populations. Inthe 1st principal component, only 2 popu-lations differed from the others (Faro andLimao). In contrast, size-free canonical dis-criminant analysis separated all popula-tions. That latter result also was found byPessoa et al. (1990:398) in populations ofthe guyannensis group from Central Braziland Amazon, leading to their propositionthat 1 population attributed to P. oris andanother attributed to P. roberti ‘‘occupy dif-ferent regions in multivariate characterspace and may represent independent evo-lutionary units.’’ Our analysis expanded thesampling of Pessoa et al. (1990), incorpo-rating 2 Cerrado samples (Fazenda Fian-

deira and Anapolis) and 5 samples from thecore extension of the guyannensis distri-bution.

Although our results were coincidentwith those of Pessoa et al. (1990), we con-sidered that divergence occurred betweenpopulations rather than between species.That was based on the following evidence:absence of morphometric separation be-tween all Cerrado populations and all east-ern Amazonian populations; the karyologic,morphologic, and molecular similarity ofthose populations; and lack of statisticaltreatment for factors that could affect phe-notypic variability among populations, suchas seasonal differences among collection of


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FIG. 4.—Scores of the first 2 canonical func-tions obtained from the size-free (5 Burnabycorrection) discriminant analysis. The symbolsfor the samples are: v Anapolis, n FazendaFiandeira, □ Faro, 1 Patagonia, V Auyan-Te-pui, l Limao, and 3 Curua-Una.

specimens (e.g., differences between indi-viduals captured in dry and humid seasons),long-term fluctuations in resource availabil-ity, and other ecological factors.

Morphologic variation.—When original-ly describing P. oris, Thomas (1904:196)commented that P. roberti ‘‘agrees veryclosely with P. oris in its cranial characters,but differs by its paler and more uniformlybuffy color, its fully haired under surface,and its much longer and softer fur, of whichthe spines form a less considerable propor-tion than usual’’ and considered that bothspecies were related to P. cayennensis (5P. guyannensis). Moojen (1948) agreedwith Thomas (1904) in distinguishing P.roberti from P. oris mainly by the consid-erably longer pelage of the former despitelack of consistent cranial differences be-tween them. When analyzing the new ma-terial, we did not find differences in pelagecharacters between specimens from easternAmazonian and Cerrado populations.

Patton (1987) reported the most exten-sive set of diagnostic characters for Proe-chimys and commented that samples from

the states of Para (Amazonian sample, P.oris) and Goias (Cerrado sample, P. ro-berti) showed broader and shallower me-sopterygoid fossae and a less developed in-fraorbital canal than other forms of the guy-annensis group. Patton (1987) showed dif-ferences between P. roberti and P. oris in2 traits: a smaller size of bacula in P. ro-berti topotypes, which was considered afunction of its overall smaller size, and dif-ferent frequencies of counterfold pattern inthe first 2 lower molars (52% of the Goiassample against 33% of the Para sample with2 folds in m1; 75% of the Goias sampleagainst 39% of the Para sample with 2 foldsin m2). In our analysis, all adult specimensfrom Fazenda Fiandeira (n 5 23) showed 2folds in both m1 and m2; 15 adults fromthe localities of eastern Para (Capim, Pata-gonia, and Tocantins localities) showed thefollowing frequencies of counterfold pat-tern: 80% with 2 folds in m1 and 73% with2 folds in m2. Those results were closer tothose found in the specimens from Goiasthan in other taxa of the guyannensis groupreported by Patton (1987). Because we didnot find a clear-cut difference in size be-tween Cerrado and Amazonian samples inour morphometric analysis, we predict thatvariation in baculum size also will be re-duced in a broader survey of bacula fromProechimys specimens of the guyannensisgroup (Patton [1987] analyzed few speci-mens from Cerrado localities).

Molecular variation.—Pairwise sequencedivergence among specimens from easternAmazonia and Cerrado populations waslow (average 5 2.44%). Divergence be-tween the Xingu and Niquelandia speci-mens (the 2 most distant sampled localitiesin eastern Amazonia and Cerrado) was only2.9%, in contrast to an average 15% diver-gence between members from those popu-lations and specimens of the guyannensisgroup north of the Amazon River.

Eighteen fundamental cladograms, eachwith 200 steps (consistency index 5 0.505,retention index 5 0.803) were obtained inthe parsimony analysis of cytochrome-b se-


FIG. 5.—Strict consensus tree of the 18 minimal length cladograms (200 steps, consistency index5 0.505, retention index 5 0.803) obtained from the analysis of the first 372 bases of mitochondrialcytochrome-b. Horizontal branch lengths are in scale; numbers above nodes indicate percentage inbootstrap analysis (only nodes with . 90%); numbers below the 3 marked nodes indicate average(and standard error) Kimura 2-parameter distances among members of the clades; numbers afterlocalities refer to map numbers in Fig. 1.

quences (Fig. 5). Samples from the Cerradoand eastern Amazonia formed a monophy-letic group supported by a high bootstrapvalue (100%). Populations from the northbank of the Amazonas River, Venezuela,and Guyana formed a 2nd clade, also sup-ported by a high bootstrap value (90%). Acorrespondence was observed betweengrouping and geographic precedence in theCerrado–eastern Amazonia clade, exceptfor 1 Xingu specimen that was nested with-in the Maraba clade. The Cerrado samplesformed a monophyletic clade with a lowbootstrap value, whereas eastern Amazonia

samples were not nested together (i.e., acladistic subdivision between Amazonianand Cerrado populations was not found inthe most parsimonious trees). Moleculardata did not support the hypothesis of 2 dif-ferent evolutionary lineages, 1 in the Cer-rado (5 P. roberti) and another in the east-ern Amazon (5 P. oris).

CONCLUSIONS

Eisenberg and Redford (1999) suggestedthat P. oris is probably a synonym of P.roberti but did not present any material ev-idence to that statement. Our results corrob-


orated that hypothesis. Lack of karyotypicdistinctiveness, low level of morphologicdifferences (expected to be even weaker ina comprehensive analysis), and lack of di-vergence between eastern Amazonian andCerrado specimens shown by moleculardata suggest that populations of the guy-annensis group from central Brazil andeastern Amazon Basin must belong to thesame taxon. Although the level of differ-entiation shown by morphometric analysiswas relatively high, this did not indicate aseparation between Cerrado and Amazo-nian populations. This differentiation mustreflect interpopulation differences, indicat-ing that phenotypic divergence among pop-ulations of the guyannensis group is higherthan karyotypic, morphologic, or geneticdivergence. Further studies accounting forother factors unrelated to geographic loca-tion are necessary to evaluate the biological(historical or ecological) factors causingthis differentiation. Inclusion of 1 samplefrom a population recognized as P. robertiin the latest review of the genus (Patton1987) and the priority of P. roberti over P.oris are the basis for assigning the formername to this species. Other named taxa ofthe guyannensis group from eastern Ama-zonia, such as arescens and boimensis, alsomay prove to belong to this same taxonom-ic taxon.

ACKNOWLEDGMENTS

We are grateful to the Instituto Brasileiro doMeio Ambiente e dos Recursos Naturais Reno-vaveis (IBAMA) for granting us with licensesfor collecting in Parque Nacional da Chapadados Veadeiros (Fazenda Fiandeira) and Bacabal(licenses 052/96, and 044/93, and 070/94). Wealso thank S. Lindbergh and B. Lemos for col-laborating with field work; R. Cerqueira for lab-oratory facilities; H. Seuanez, R. S. Voss, and 2unknown referees for reviewing previous ver-sions of the manuscript; L. Flamarion (MN, Riode Janeiro), R. S. Voss (AMNH, New York), andD. Oren (MPEG, Belem) for access to collec-tions; and J. L. Patton and M. N. F. da Silva forkindly providing the cytochrome-b sequencedata. Work was supported by IBAMA, Conselho

Nacional de Desenvolvimento Cientıfico e Tec-nologico (CNPq), Coordenacao de Amparo aPos Graduacao e Ensino Superior (CAPES),Fundacao de Apoio a Pesquisa do Estado do Riode Janeiro (FAPERJ), and INCa-FAF (Brazil).

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Submitted 8 February 1999. Accepted 14 April 2000.

Associate Editor was Meredith J. Hamilton.

STATUS OF PROECHIMYS ROBERTI AND P. ORIS (RODENTIA: ECHIMYIDAE) FROM EASTERN AMAZONIA AND CENTRAL...

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Transcript of STATUS OF PROECHIMYS ROBERTI AND P. ORIS (RODENTIA: ECHIMYIDAE) FROM EASTERN AMAZONIA AND CENTRAL...