Neacomys minutus, PATTON & DA SILVA & MALCOLM, 2000

PATTON, JAMES L., DA SILVA, MARIA NAZARETH F. & MALCOLM, JAY R., 2000, Mammals Of The Rio Juruá And The Evolutionary And Ecological Diversification Of Amazonia, Bulletin of the American Museum of Natural History 2000 (244), pp. 1-306 : 105-113

Neacomys minutus , new species

HOLOTYPE: INPA 2689 (Instituto Nacional de Pesquisas da Amazônia, Manaus), adult female (lactating and pregnant, with three embryos), collected 17 November 1991 by James L. Patton (original number 16073); skin with skull and mandibles, in good condition; liver and kidney tissue preserved in 95% ethyl alcohol and maintained in the tissue collections of both INPA and the Museum of Vertebrate Zoology , University of California, Berkeley ( MVZ).

TYPE LOCALITY: Altamira, left bank Rio Jurua´, Amazonas, Brazil, 6°35'S, 68°54'W Obtained in terra firme forest on our standardized trap line in a Sherman live trap, station number D­ 14.

DIAGNOSIS: This is a diminutive species with a long tail, dark orange dorsal coloration strongly but finely streaked with black (fig. 68), short ears (13 mm or less), small and delicate skull (figs. 70, 71, 76), short maxillary toothrow (<2.75 mm), primitive carotid arterial system (pattern 1 of Voss, 1988; Carleton and Musser, 1989) with a squamoso­alisphenoid groove and sphenofrontal foramen, incisive foramen teardrop in shape (fig. 74), a weakly developed anteromedian flexus (­id) of both upper and lower first molars (fig. 72), and karyotype of 2n = 35–36, FN = 40 (fig. 75B­C).

REFERRED SPECIMENS: We obtained 31 additional specimens from seven localities within the Rio Jurua´, including the type locality. These include Sacado (locality 5)— MNFS 624 (adult female, skin with skull) and 642 (adult male, fluid) ; Penedo (locality 7)—JLP 15356 (adult male, skull with body in fluid), JLP 15365 (adult male, skin with skull), MNFS 376 (adult male, skull with body in fluid), MNFS 409 (adult female, skin with skull), MNFS 410 (adult female, fluid) MNFS 493 (subadult male, complete skeleton), MNFS 494 (adult male, complete skeleton) ; Nova Empresa (locality 8)—JUR 3 (adult female, skull only), JUR 48 (adult male, skull with body in fluid) ; Altamira (locality 9)—JLP 16046 (adult male, fluid), JLP 16059 (adult female, fluid), JLP 16060 (adult female, skin and skull), JLP 16061 (adult male, skin with skull), JLP 16062 (subadult male, fluid), JLP 16063 (adult male, fluid) JLP 16064 (adult female, fluid), JLP 16065 (adult female, fluid), JLP 16078 (adult male skin with skull), JLP 16079 (adult female skin with skull) ; Barro Vermelho (locality 12)—JLP 15846 (adult female, skin with skull), JLP 15847 (adult male, skin with skull) ; Vira­Volta (locality 14)–JUR 487 (adult female, skin with skull), MNFS 1718 (adult male, skull with body in fluid), MNFS

1734 (adult female, fluid), MNFS 1735 (adult female, skin with skull), MNFS 1742 (adult male, fluid), MNFS 1743 (adult female, skull with body in fluid), MNFS 1744 (adult male, skull with body in fluid), MNFS 1745 (adult male, fluid); and Ilhazinha (locality 16)—MNFS 1787 (adult female, fluid).

MEASUREMENTS OF HOLOTYPE: TOL, 145; TAL, 74; HF, 20; E, 12; CIL, 17.49; ZB, 10.44; MB, 8.54; IOC, 4.11; RL, 6.36; NL, 7.27; RW­1 , 3.93 ; RW­2 , 3.12 ; OL, 6.67; D, 5.10; MTRL, 2.42; IFL, 2.90; PBL, 7.75; AW, 3.91; OCB, 4.92; BOL, 2.92; MPFL, 2.68; MPFW, 1.74; ZPL, 1.87; CD, 7.09.

ADDITIONAL MEASUREMENTS: See table 24.

DESCRIPTION AND COMPARISONS: This is the second small­bodied species in the Rio Juruá basin (skin, fig. 68; skull, figs. 70­71; table 24). Although these two are not sympatric (fig. 64), N. minutus is readily distinguished from N. musseri by a number of cranial char­

acters and by karyotype, as well as by molecular sequences. It is smaller in virtually all external and cranial measurements, except with a slightly longer and much broader mesopterygoid fossa (table 24). It possesses the primitive carotid arterial system characteristic of other members of the genus, as opposed to the derived condition in N. musseri The incisive foramen is distinctly teardrop in shape, rather than oval, with a narrower septum (fig. 74). The anteromedian flexus (­id on both upper and lower first molars is weakly developed (fig. 72). And it has a 2n = 35– 36, FN = 40 karyotype versus the 2n = 34 FN = 64–68 of N. musseri . Neacomys minutus does not differ appreciably, however in cranial shape parameters, maintaining the same proportionality of length, width, and height as in N. musseri . This is evident in both bivariate plots of individual measurements as well as in the principal components analysis. Although the two species differ substantially in overall size (as evidenced by their respective scores on PC­1 axis; table 24), their significant difference on PC­2 is due solely to mesopterygoid fossa width, and they are statistically identical on all subsequent PC axes (table 24). Neacomys minutus is considerably smaller that N. spinosus in all external and cranial measurements, but shares with it the primitive carotid arterial pattern. The distinctly small hind feet, black instead of more brown ears, and darker dorsal pelage more finely streaked with black are characters useful for field separation of these two species, other than general body size.

DISTRIBUTION AND HABITAT: Known only from the central (Upper Central and Lower Central regions) and lower (Mouth Region sections of the Rio Jurua´, Estado do Amazonas, Brazil (fig. 62). Small­bodied taxa of generally similar morphology from adjacent areas in northern Perú and eastern Ecuador (clade 3, fig. 63), or on the opposite (northern) side of the Rio Solimões along the Rio Jaú in central Brazil (clade 6, fig. 63), belong to quite different mtDNA clades and are probably best considered to be separate species. We caught these mice in terra firme forest at localities 7, 9, 12, 14, and 16, but in seasonally flooded várzea forest at localities 5 and 8.

REPRODUCTION: We caught pregnant females in the months of August, September, October, November, May, and June. These span both the dry and wet seasons, and suggest that reproduction is yearround. Litter sizes were three in all cases. One female was both lactating and in the early stages of pregnancy, suggesting a postpartum estrus. Individuals of both sexes were in reproductive condition (pregnant females and males with scrotal testes and enlarged vesicular glands) while still partly in subadult pelage and with completely erupted but unworn molar teeth suggesting that breeding commences at an early age.

ETYMOLOGY: Named for its distinctly small size and diminutive features.

KARYOTYPE: 2n = 35–36, FN = 40 (fig 74B­C). The autosomes consists of 14 pairs of acrocentric elements, three distinctly large, one medium­sized, and the remainder grading in size from small to very small. The medium­sized element is apparently involved in a Robertsonian polymorphism, with heterozygous individuals found at both Sacado (locality 5) and Altamira (locality 9); all others (from Penedo [locality 7], Barro Vermelho [locality 12], and Vira­Volta [locality 14]) were homozygous for the acrocentric condi­ tion. There are also three pairs of very small biarmed autosomal elements. The X­chromosome is a medium­small metacentric chromosome; the Y­chromosome is small and acrocentric.

COMMENTS: This species is morphologically similar to small­bodied Neacomys that we have examined from northern Perú and Ecuador (clade 6, fig. 63), although the two differ greatly in molecular sequence. The average Kimura two­parameter distance be­ tween these samples is 13.05% (table 23). Although it might be argued that this difference is due in part to the geographic distance between the samples, N. spinosus exhibits only 2% divergence among samples taken across the same large geographic region. Moreover, phylogenetic analyses provide no support for a sister­group relationship between the Rio Juruá and northwestern Amazonian forms, relative to any other identifiable clade (fig. 63).

This taxon also exhibits considerable geographic differentiation in cytochrome­b sequences within the Rio Juruá basin (fig. 64) Specimens from the Upper Central localities of Seringal Condor (6) and Penedo (7) differ on average, from those from the Lower Central and Mouth regions (Altamira [9], Barro Vermelho [12], Vira­Volta [14], and Ilhazinha [16]) by 6.9% (table 23), with great similarity of haplotypes within each of these two geographic clusters (0.41%, or less). Com­

parisons between the limited samples of the two clades (9 adults for the upriver clade, 11 for the downriver clade) in morphometric characters revealed no significant differences for any single variable. Nevertheless, specimens belonging to the two clades are separable based on multivariate discriminant analysis, with the mean scores on the single discriminant axis significantly different (F 1,18 = 109.772, p <0.001). Table 25 lists the standardized discriminant coefficients for the 16 variables included in the analysis, and figure 76 provides a histogram of the scores for individuals of both clades on the single discriminant axis extracted. This analysis correctly classifies all 20 individuals to their respective cytochrome­b clades, despite what appears to be rather minimal separation on the single axis obtained in the analysis (fig. 77). For the moment, we assign no special taxonomic significance to this difference, although such may be supported by additional samples. Rather, we only highlight this difference, both to illustrate the parallel pattern of differentiation in molecular as well as morphological characters and to further emphasize the number of strongly defined and differentiated haplotype clades of small­bodied Neacomys that apparently replace one another across Amazonia.

Neacomys spinosus (Thomas, 1882)

TYPE LOCALITY: ‘‘Huambo, 3700',’’ to the east of Chachapoyas and Chirimoto, on the banks of the Río Huambo, a tributary of the

Huallaga (Thomas, 1882: 99), Departamento de Amazonas, Peru´.

DESCRIPTION: This is the largest species in the genus, averaging over 180 mm in total length and 20.7 mm in condyloincisive length of the skull (table 24, figs. 69 and 70) From eastern Ecuador to southern Perú and east into western Brazil, N. spinosus is relatively uniform in body dimensions, but exhibits variation in the darkness of the dorsal pelage, ranging from a paler yellow­reddish brown mixed with black to a darker reddishbrown. An appreciation of this type of variation must await a more detailed and thorough analysis. Within our sample from the Rio Jurua´, the skull is long with a relatively narrow braincase, but it differs only in general size, rather than in proportions, from other species in the genus (fig. 73, and above). The carotid circulation pattern is of the primitive type, retaining the well­developed squamosal­alisphenoid groove and sphenofrontal foramen indicative of the presence of the supraorbital branch of the stapedial artery (pattern 1; Voss, 1988; Carleton and Musser, 1989). The maxillary toothrow is longer than that of other species, averaging over 3 mm in length. The molar occlusal morphology is similar to that of other species (fig. 72), except that the procingulum of both upper and lower first molars is either entire or only weakly divided into anterolabial and anterolingual conules by the anteromedian flexus (­id).

SELECTED MEASUREMENTS: See table 24.

DISTRIBUTION AND HABITAT: Specimens that can be clearly allocated to this species are known from southeastern Colombia south through eastern Ecuador and Perú into northern Bolivia, and east as far as the central Rio Juruá basin in Estado do Amazonas Brazil (figs. 62 and 63; table 22). Along the Rio Jurua´, we obtained specimens only in the Headwaters (localities 1, 2, and 4) and Upper Central regions (localities 6 and 7). In the former, both nonflooded terra firme and periodically flooded ‘‘várzea’’ forests were occupied, but the species is apparently limited to terra firme further downriver.

KARYOTYPE: 2n = 64, FN = 68 (fig. 75D) We have data from 13 individuals from four localities: Porongaba (locality 1: MNFS 1236, 1262, 1263, 1322, 1404), opposite Po­

rongaba (locality 2: MNFS 1339), Sobral (locality 4: MNFS 1481, 1565), Condor (locality 6: JLP 15674), and Penedo (locality 7: JLP 15292, 15314, MNFS 348, 357). The autosomal complement is almost entirely acrocentric, with one distinctly large pair, four pairs of medium size, and 23 pairs that grade from small to very small. There are also three pairs of very small biarmed elements. The X­chromosome is a medium­large subtelocentric chromosome, and the Y­chromosome is a very small acrocentric element. This karyotype is identical to that described from specimens collected in Colombia and several localities throughout Perú (Gardner and Patton, 1976).

REPRODUCTION: Three of 12 females taken during August and September in the dry season were pregnant, with two or three embryos; others were either nulliparous young or postlactating without signs of current reproductive activity. Four of eight females taken in the months of February and March, during the rainy season, were pregnant (embryo count ranging from 2 to 4), two were postlactating, and two were young of the year.

COMMENTS: This species appears to be rather uniform in body size throughout its range in western Amazonia, and thus readily distinguishable by this feature alone from the various sympatric, small­bodied forms described above. The level of mtDNA sequence divergence across its sampled geographic range is also limited, with an average divergence of only 2.1% among specimens from eastern Ecuador, northern Peru´, and the Rio Juruá basin. The maximum Kimura two­parameter distance between any two haplotypes is 3.7% (a specimen from Ecuador and one from the Rio Jurua´). There is essentially no differentiation between localities within the Rio Jurua´, with greater variation among haplotypes within some localities (e.g., Sobral, locality 4) than among them (fig. 65). Names available that are probable synonyms of N. spinosus include amoenus Thomas (1903) and carceleni Hershkovitz (1940).

SPECIMENS EXAMINED (n = 33): (1) 5f — MNFS 1236, 1262–1263, 1322, 1404; (2) 1f — MNFS 1339; (4) 3f — MNFS 1438, 1481, 1565; (6) 1m — JLP 15674; (7) 10m, 13f — JLP 15292, 15314, 15341–15344, 15364, 15457, 15497, MNFS 348, 357–359, 374, 375, 377–379, 407, 424–425, 473, 523