Proechimys J. A. Allen, 1899

VOSS, ROBERT S., LUNDE, DARRIN P. & SIMMONS, NANCY B., 2001, The Mammals Of Paracou, French Guiana: A Neotropical Lowland Rainforest Fauna Part 2. Nonvolant Species, Bulletin of the American Museum of Natural History 2001 (263), pp. 1-236 : 155-164

Proechimys J. A. Allen

The last comprehensive revision of the genus Proechimys was Moojen’s (1948) monograph, but subsequent research has resulted in substantial modifications of his pioneering taxonomic synthesis. In particular, studies of well­sampled local faunas have proven crucial for distinguishing patterns of morphological, karyotypic, and molecular variation within and among sympatric species of Proechimys , especially in western Amazonia where four or more occur at some localities (Patton and Gardner, 1972; da Silva, 1998; Patton et al., 2000). To date, however, no equivalent studies of character variation within and among sympatric Proechimys species from other Amazonian subregions have been published.

Until quite recently, only a single widespread species of Proechimys , variously identified as P. guyannensis (E. Geoffroy, 1803) or as P. cayennensis (Desmarest, 1817) , was recognized in the Guianas (e.g., by Tate, 1935; Cabrera, 1961). In 1978, however, A. M. Husson (at the Rijksmuseum van Natuurlijke Historie, Leiden) and F. Petter (at the Muséum National d’Histoire Naturelle, Paris) independently reported the occurrence of two sympatric forms in Surinam and in French Guiana, respectively. Although both authors recognized a common large species and a rarer small species, they gave different accounts of diagnostic nonmetrical characters and they used different nomenclature.

Husson (1978) identified his large Surinamese specimens as Proechimys guyannensis (E. Geoffroy, 1803) , and his small specimens as P. warreni Thomas (1905) . In Husson’s opinion, measurements of the cheekteeth provided the best diagnostic criterion: 18 specimens of the large Surinamese species had maxillary toothrow lengths of 8.3– 9.2 mm, whereas 6 specimens of the small species had cheektooth measurements of 7.2–7.7 mm. Husson also reported that his large species was more abundant, and had more rufous pelage, a relatively shorter tail, less appressed caudal hairs, and a wider mesopterygoid notch in the back of the hard palate than his small species (op. cit.: 429– 438). Husson based his identification of the large species primarily on Geoffroy’s (1803) description of pelage color in guyannensis because the skull of the type (not measured by Geoffroy) was thought to have been lost (Rode, 1945). Husson’s identification of the small species, however, was based on direct external and craniodental comparisons with the type of warreni .

Petter (1978) reported the rediscovery of the type skull of Proechimys guyannensis and assigned this name to the smaller (and rarer) of the two forms found in French Guiana; the larger (and more abundant) form, apparently undescribed, was then named as a new species, P. cuvieri . However, whereas Husson found that the large and small Surinamese species were nonoverlapping in maxillary toothrow length, Petter reported overlapping variation in this measurement, with observed ranges of 7.0– 8.5 mm for guyannensis and 8.1–9.3 mm for cuvieri . Petter did not mention the other distinguishing characters discussed by Husson, but he noted karyotypic differences (2N = 40 in guyannensis , 2N = 28 in cuvieri ) and differences in the number of enamel islands of the lower cheekteeth (two per tooth in guyannensis , three in cuvieri ). The karyotypes of guyannensis and cuvieri were subsequently described in greater detail by Reig et al. ( 1979).

In an important review of morphological variation in Proechimys, Patton (1987) identified several qualitative characters distinguishing clusters of populations assigned to his cuvieri and guyannensis species groups. However, Patton’s study included no French Guianan material, so the diagnostic value of the characters he investigated is unknown for the local populations sampled by our study. Indeed, Guillotin and Ponge (1984: 287) doubted that cuvieri and guyannensis could be distinguished by ‘‘méthodes morphologiques classiques’’, a conclusion based on bivariate and multivariate analyses that showed no obvious morphometric discontinuity among French Guianan specimens representing both of the karyomorphs reported by Petter (1978) and Reig et al. ( 1979). The apparent lack of diagnostic external characters between guyannensis and cuvieri has also been an impediment for ecologists unable to identify these species by nondestructive sampling in field studies (e.g., Forget, 1991).

The morphological characters of French Guianan populations of Proechimys cuvieri and P. guyannensis are important because both species are based on types collected in French Guiana (Petter, 1978). Additionally, the application of these names to the sympatric Surinamese forms reported by Husson remains to be evaluated. In order to identify our Paracou vouchers, and to provide a basis for future revisionary research with these species, we examined most of the Proechimys specimens from French Guiana currently held in American and European museums. Except as noted below, our results are based on measurements and qualitative character data obtained from fully adult but nonsenescent animals, herein defined as members of age categories 8 and 9 of Patton and Rogers (1983). The following results of our analyses broadly overlap those independently obtained by Catzeflis and Steiner (2000), who examined many of the same specimens.

Maxillary toothrow measurements of nonsenescent adult Proechimys from French Guiana form two distributions (fig. 76): a sparse cluster of small specimens with cheekteeth measuring 6.9–8.0 mm, and a denser cluster of larger specimens with longer tooth­

TABLE 45 Measurements (mm) and Weights (g) of Adult Proechimys cuvieri and P. guyannensis from French Guianaa

rows (8.2–9.3 mm). Following Petter (1978), we associate the name guyannensis with the smaller­toothed form based on the toothrow dimensions of the holotype (MNHN 1995.1395, an old adult), which has an alveolar measurement of 7.8 mm and an estimated crown measurement of 7.3 mm (table 45). The larger­toothed specimens that we measured include the type of cuvieri, MNHN 1977.774, which has a crown­length toothrow measurement of 8.5 mm. To supplement this essentially univariate distinction, we examined qualitative variation in craniodental, external, and genitalic characters to determine whether or not Proechimys with small versus large cheekteeth differ in other respects.

We scored the septum that separates the right and left incisive foramina as ‘‘complete’’ or ‘‘incomplete’’ (fig. 77). Variation in this character among the specimens at hand is determined by the presence or ab­ sence of contact between the bony capsules containing Jacobson’s organ and a median process of the maxillary bone. Initially, we distinguished complete septa formed by slen­ der maxillary processes from complete septa formed by robust maxillary processes, but intermediate conditions made this additional refinement too arbitrary for confident scoring.

We scored the development of the canal transmitting the infraorbital nerve in the floor of the infraorbital foramen (fig. 78) using the numerical coding suggested by Patton (1987): no groove present (1), or groove moderately developed (2), or groove well defined (3). Scoring these conditions as well as intermediate states (1.5, 2.5) was accomplished by reference to exemplar specimens of Brazilian Proechimys guyannensis previously examined by J. L. Patton (personal commun.). Therefore, we presume that our trait­frequency data and his (Patton, 1987: table 3) are comparable.

We also followed Patton’s (1987) numerical coding convention for the depth of the mesopterygoid fossa (fig. 77): not extending to the posterior margin of M3 (1), or extending to the posterior half of M3 (2), or extending to the anterior half of M3 (3), or extending to the posterior half of M2 (4), or extending to the anterior half of M2 (5). Because the angle formed by the posterior palatal margins of the mesopterygoid is correlated with the depth of penetration of the fossa between the toothrows (deeper fossae have more acutely angled palatal margins; Patton, 1987), we did not score the shape of the mesopterygoid notch as a separate character.

Finally, we recorded the number of internal folds on the second mandibular molar (corresponding to the ‘‘îlots d’émail’’ of Petter, 1978); compound (Y­shaped) folds were each counted as one­and­a­half folds. As not­ ed by Patton (1987), internal fold number and morphology change with toothwear, so it is particularly important that this character be scored among individuals of approximately equivalent age.

Trait frequencies of these four qualitative characters differ significantly between our operationally defined samples of cuvieri (with MTR Ź 8.2 mm) and guyannensis (with MTR ± 8.0 mm) despite the small number of guyannensis available for scoring (table 46). The presence or absence of a complete incisive septum and the development of an infraorbital groove are the two qualitative characters most consistently correlated with maxillary toothrow length: all large­toothed specimens ( cuvieri ) have a complete incisive septum and either lack an infraorbital groove entirely or have a very weakly defined groove; by contrast, most small­toothed specimens have an incomplete incisive septum and well­defined infraorbital grooves. Although most specimens of both tooth­size classes have a moderately deep mesopterygoid fossa and 2 ½ folds on m2, no specimens of small­toothed rats in our sample have either a very shallow mesopterygoid fossa or m2s with 3 folds. It is noteworthy that the qualitative traits of the specimen with a maxillary toothrow length of 8.0 mm (MNHN 1981.48, which could be interpreted as an outlier of either tooth­size class) link it unambiguously with guyannensis , and that specimens with ‘‘atypical’’ states for one qualitative character (e.g., AMNH 267047, a small­toothed animal that lacks any trace of an infraorbital groove) are not atypical in other qualitative respects. Altogether, these results strongly support the hypothesis that the discrete tooth­size classes associated with the names cuvieri and guyannensis represent valid species, a conclusion that is further bolstered by external, genitalic, and karyotypic comparisons.

As noted by Malcolm (1992), the tail of Proechimys cuvieri is visibly hairier than that of P. guyannensis . This difference is caused by the individual caudal hairs, which curve outward from beneath each epithelial scale in P. cuvieri , where they can easily be seen standing away from the caudal surface (fig. 79, left). By contrast, the individual hairs are appressed to the caudal surface in P. guy­

by moderately developed lateral flange ( P. cuvieri [AMNH 266574] scored as ‘‘2’’); C, nerve canal present, defined by highly developed lateral flange ( P. guyannensis [AMNH 266595] scored as ‘‘3’’).

TABLE 46 Comparisons of Qualitative Character­State Frequencies Between Proechimys cuvieri and P. guyannensis a

annensis, where they are difficult to see without magnification; in consequence, the tail appears to be smooth and naked (fig. 79, right).

The dorsal body pelage of Proechimys cuvieri is, on average, redder (more saturated) than the generally drab (grayish or yellowish brown) fur of P. guyannensis , but there is sufficient overlap in color among the specimens at hand that this contrast is useful for field identification only in combination with size and other characters. This seems to be the only significant species color difference in the material we examined. For example, we did not see any diagnostically useful differences in ventral fur color (pure white in most specimens of both species), tail pig­ mentation (distinctly bicolored in most specimens of both species), or hindfoot markings.

The male genitalia differ strikingly in shape between Proechimys cuvieri and P. guyannensis . Whereas the penis of cuvieri is short and very broad, that of guyannensis is long and slender, an obvious contrast that is reflected in the highly divergent bacular morphologies illustrated by Patton (1987: figs. 5, 10) for members of his cuvieri and guyannensis species groups. Although this character cannot be used to identify most museum study skins (few of which have the penis attached), it is potentially useful for field identifications because the penis can be extruded by retracting the prepuce of live animals.

Karyotypic data recorded on skin tags of MNHN specimens indicate that different diploid counts are associated with the divergent morphological phenotypes described above and corroborate Petter’s (1978) and Reig et al.’s ( 1979) taxonomic assignments. Thus, five French Guianan specimens that we examined with recorded karyotypes of 2N = 28 (MNHN 1972.639, 1974.263, 1974.266, 1981.36, 1998.315) represent the cuvieri morphotype, whereas two specimens that we examined with 2N = 40 (MNHN 1983.376, 1998.312) represent the guyannensis morphotype.

In the following species accounts we summarize diagnostic characters, comment on Husson’s (1978) identifications of Surinamese material, and evaluate the probable geographic distribution of Proechimys cuvieri and P. guyannensis based on our assessment of character variation in the material at hand.

Proechimys cuvieri Petter Figures 77–80

VOUCHER MATERIAL: AMNH 266570– 266575 , 266578 , 266580–266582 , 266588 , 266589 , 266591 , 266592 , 266594 , 267025– 267030 , 267032 , 267034 , 267039 , 267041 , 267045 , 267599 , 267601–267603 , 269122 ; MNHN 1998.685 – 1998.699 . Total = 46 specimens .

IDENTIFICATION: Based on the preceding synthesis of character data from French Guianan material, adult specimens of Proe­

chimys cuvieri can be characterized as large rats that contrast with adults of the smaller sympatric species P. guyannensis by their longer (Ź 8.2 mm) maxillary toothrows (versus ±8.0 mm in guyannensis ), complete incisive septum (vs. septum usually incomplete in guyannensis ), incisive foramina with larg­ er posterolateral flanges (vs. foramina usually with smaller flanges in guyannensis ), palatal bridge with better developed median keel (vs. palate unkeeled or weakly keeled in guyannensis ), infraorbital groove absent or usually weakly developed (vs. groove usually well developed in guyannensis ), mesopterygoid fossa often shallow and broad (vs. deeper and narrower in many guyannensis ), lower molars usually with more than two internal folds (vs. lower molars often with two folds in guyannensis ), tail visibly hairier (vs. apparently smooth and naked in guyannensis ), pelage often reddish (vs. drab in most guyannensis ), penis short and very broad (vs. longer and narrower in guyannensis ), and diploid karyotype with 28 chromosomes (vs. 2N = 40 in guyannensis ).

In our experience, fully adult Proechimys in French Guiana can be identified to species in the field with considerable confidence using external measurements (e.g., hindfoot length, table 45) and the qualitative external traits described above. However, taxonomic assignments of juvenile and subadult Proechimys (with unmolted or incompletely molt­ ed soft, gray, immature pelage) are always problematic. Tooth impressions (Malcolm, 1992) and molecular markers (Steiner et al., 2000) are potentially useful tools for identifying young animals that should be incorporated in future field studies. Otherwise, many individuals will inevitably remain unidentified in ecological research based on nondestructive sampling, especially during the rainy season, when a considerable fraction of the population consists of young animals (Guillotin, 1982).

Specimens that we examined document the sympatry of Proechimys cuvieri and P. guyannensis at several localities in French Guiana, including Arataye, Cayenne, Florida, Montsinéry, and St.­Eugène, as well as Paracou. We presume that these species are also co­distributed elsewhere, certainly in Suri­ nam and perhaps throughout the Guiana subregion of Amazonia.

According to Patton et al. (2000), Proechimys cuvieri is widely distributed in Amazonia, including large parts of the Guianan, southeastern, and western subregions. Although cuvieri is said to be relatively uniform in morphological characters throughout this enormous range, significant mtDNA sequence divergence (7–9%) exists among several geographic clusters of populations sampled by those authors (op. cit.). We have not attempted to evaluate geographic variation among Amazonian populations of cuvieri ­ like spiny rats for this faunal report, but it is relevant to note that typical (French Guian­ an) cuvieri appears to differ significantly from western Amazonian material in some morphological traits. For example, whereas Patton et al. (2000) reported that the vomer (an element of the incisive septum) is exposed in most (25 out of 34) specimens from the Rio Jurua´, this bone is not exposed in any of our 22 adult Paracou vouchers. If geographic patterns of variation in this and other morphological characters were found to be consistently correlated with mtDNA haplotype divergence, it would be reasonable to infer that two or more species could be represented among the samples currently referred to this species.

REMARKS: Husson (1978) identified Surinamese material of this species as Proechimys guyannensis on the basis of Geoffroy’s (1803) and Desmarest’s (1817) color descriptions of the type, and on the assumption that the type of guyannensis probably represented the commoner of the two Guianan forms. Color alone, however, is not a reliable basis for species identification, and the other morphological details mentioned in Geoffroy’s and Desmarest’s descriptions are likewise insufficient to determine which local species they had in hand. Petter’s (1978) rediscovery of the long­lost type skull of P. guyannensis finally resolved the identity of that taxon and indicated the necessity of naming the larger form as a new species.

OTHER SPECIMENS EXAMINED: French Guiana — Arataye ( MNHN 1983.378 ; USNM 548450–548452 ), Cacao ( MNHN 1981.107 ), Cayenne ( MNHN 1970.223 , 1974.263 ), Florida ( MNHN 1981.46 , 1981.50 ), Piste St. ­Élie ( MNHN 1982.523 ), St.­Eugène ( MNHN 1995.3220 – 1995.3222 , 1995.3224 , 1998.314 , 1998.315 , 1998.1821 ), Saül ( MNHN 1977.774 [holotype], 1981.23, 1981.24, 1981.26, 1981.29 –1981.33, 1981.36), Station FRG near Montsinéry ( MNHN 1986.1129 ), Trois­Sauts ( MNHN 1981.54 , 1981.56 ), no other locality data ( MNHN 1972.639 , 1974.266 ) .

FIELD OBSERVATIONS: All of our unambiguous records of Proechimys cuvieri from Paracou are based on collected specimens. Of our 46 vouchers, 18 (39%) were taken in Sherman traps, 14 (30%) were shot, 7 (15%) were taken in Victor traps, 4 (11%) were taken in Tomahawk traps, 2 (4%) were taken in Conibear traps, and 1 was taken in a pitfall. Forty­four specimens (96%) were shot or trapped at ground level, but 2 specimens (4%) were taken in traps tied to lianas 0.7– 1.0 m above the ground. Habitat data record­ ed for 45 specimens include 10 captures (22%) in well­drained primary forest, 3 captures (7%) in swampy primary forest, 10 captures (22%) in creekside primary forest, 2 captures (4%) in primary forest of unspecified character, and 20 captures (44%) in secondary vegetation. Microhabitat notes accompanying 28 specimens trapped at ground level record captures made under masses of fallen branches and other debris (8 specimens), under logs (5), in unsheltered sites in dense understory vegetation (5), beside logs (3), at the bases of trees (2), among stilt roots (1), on top of a log (1), inside a hollow log (1), on a smooth branch fallen over a stream (1), and under an overhanging stream bank (1).

Proechimys guyannensis (E. Geoffroy) Figures 77–80

VOUCHER MATERIAL: AMNH 266576 , 266577 , 266586 , 266595 , 267037 , 267038 , 267047 ; MNHN 1998.682 – 1998.684 . Total = 10 specimens .

IDENTIFICATION: External and craniodental characters that distinguish this species from Proechimys cuvieri in French Guiana are discussed above and need not be repeated here.

Patton (1987) mapped the distribution of the guyannensis species group of Proechimys as extending throughout eastern Amazonia together with adjacent parts of the northern Venezuelan coast and the Brazilian Cerrado. Besides the type species, Patton listed the following taxa as group members: cherriei Thomas , roberti Thomas , vacillator Thomas, oris Thomas , warreni Thomas , boimensis Allen, arescens Osgood, riparum Moojen, and arabupu Moojen (see Cabrera, 1961, for bibliographic references). Patton believed that more than one valid species was represented by these names, emphasizing morphological differences between samples from the Guiana subregion (for which the oldest available name is guyannensis ), and those from south of the Amazon (for which the oldest name is roberti ).

The morphological trait frequencies reported herein for typical Proechimys guyannensis (from French Guiana) resemble those tabulated by Patton (1987) for guyannensis ­ group samples from north of the Amazon, which we provisionally regard as conspecific. By contrast, specimens from southeastern Amazonia have divergent trait frequencies (op. cit.) and also differ from north­bank samples in karyotypes and cytochrome­b sequences (Weksler et al., 2001). Apparently, all recently collected Proechimys from Venezuelan coastal rainforests (north of the Orinoco) are referable to other species groups (Aguilera and Corti, 1994; Aguilera et al., 1995; Corti and Aguilera, 1995). Therefore, P. guyannensis appears to be an Amazonian endemic largely, but perhaps not exclusively, distributed in the Guiana subregion. 23

23 The type locality of Echimys cherriei Thomas , a taxon listed by Patton (1987) as a member of the guyannensis species group, was incorrectly mapped (op. cit.: fig. 1) in the easternmost coastal rainforest region

REMARKS: Surinamese material of this species was identified as Proechimys warreni by Husson (1978), who used the name P. guyannensis for the larger species identified as P. cuvieri in this report (see the preceding account).

Although Proechimys guyannensis (Geoffroy, 1803) has long been recognized as a valid name (e.g., by Moojen, 1948; Hershkovitz, 1948b; Cabrera, 1961; Patton and Gardner, 1972; Patton, 1987), this epithet was rejected as unavailable by Woods ( 1993), who used the replacement name cayennensis Desmarest (1817) instead. In our opinion, Mus guyannensis and other names first published by Geoffroy (1803) are unambiguously available from that work for the reasons clearly explained by Hershkovitz (1955) and Holthuis (1963).

OTHER SPECIMENS EXAMINED: French Guiana — Arataye ( MNHN 1983.381 ; USNM 548454 –548456 ), Cayenne ( MNHN 1983.374 , 1983.376 , 1995.1395 [holotype]), ‘‘Fleuve Oyapock’’ ( MNHN 1983.375 ), Florida ( MNHN 1981.48 , 1982.601 ), Montsinéry ( MNHN 1986.1124 ), Nancibo ( MNHN 1986.1130 ), Petit Saut ( MNHN 1998.312 ), St.­Eugène ( MNHN 1994.128 ), no other locality data ( MNHN 1981.88 , 1981.103 ) .

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of northern Venezuela, where only P. trinitatis is currently known to occur (see range maps in Aguilera and Corti [1994], Aguilera et al. [1995], and Corti and Aguilera [1995]). In fact, the type locality of cherriei is Munduapo (= Monduapo according to Paynter, 1982), on the right bank of the upper Orinoco at 4°54̍N, 67°48̍W in the Guiana subregion of Amazonia.

Other concepts of Proechimys guyannensis are not consistent with the taxonomic and geographic limits recognized in this report. In particular, the synonymy of P. cayennensis (= P. guyannensis in our usage) provided by Woods ( 1993) includes columbianus Thomas (a member of Patton’s [1987] semispinosus species group); hylaea Moojen, leioprimna Moojen, nesiotes Moojen, and rattinus Thomas (members of Patton’s goeldii species group); ochraceus Osgood (a member of Patton’s trinitatus species group); and villacauda Moojen (a member of Patton’s longicaudatus species group). Apparently, Woods’ association of these nominal taxa with guyannensis followed Moojen’s (1948) generic revision, a historically important but now outdated reference. Unless shown to be incorrect by subsequent research, Patton’s carefully documented allocations of nominal taxa to species groups should be used as the basis for all future classifications of Proechimys .

TABLE 47 Comparison of Capture­Habitat Frequencies between Proechimys cuvieri and P. guyannensis Trapped at Paracoua

FIELD OBSERVATIONS: All of our definite records of Proechimys guyannensis at Paracou are based on collected specimens. Of our 10 vouchers, 3 (30%) were captured in Victor traps, 5 (50%) in Sherman traps, and 2 (20%) were shot. Eight of our vouchers (80%) were shot or trapped on the ground, but 2 (20%) were taken in traps tied to lianas 0.5–1.6 m above the ground. Recorded habitat data include 9 captures (90%) in welldrained primary forest and 1 (10%) in creekside primary forest. By comparison with Proechimys cuvieri , which we caught with almost equal frequency in primary forest and secondary growth, P. guyannensis was captured significantly more often in primary forest (table 47).

Figures

Fig. 77. Morphology of the incisive foramina and the posterior palate in Proechimys guyannensis (A, AMNH 266595) and P. cuvieri (B, AMNH 266592). Whereas the bony septum that separates the right and left incisive foramina is usually incomplete in P. guyannensis, the septum is always complete in P. cuvieri. Additionally, the incisive foramina of P. cuvieri are usually constricted posteriorly by well­developed lateral flanges of the maxillary bone, the posterior palate often has a prominent median keel, and the mesopterygoid fossa is typically broad and shallow. By contrast, the bony relief of the posterior palate is less prominent in most specimens of P. guyannensis, in which the mesopterygoid fossa is often narrower, more acutely angled, and penetrates farther between the toothrows. Scale bar = 5 mm.

Fig. 78. Morphology of the floor of the infraorbital foramen in French Guianan Proechimys, illustrating alternative conditions of the canal for the infraorbital nerve scored as character states in table 46. A, Floor of infraorbital foramen smooth, without nerve canal (P. cuvieri [AMNH 266572] scored as ‘‘1’’); B, nerve canal present, defined

Fig. 79. Caudal pelage of Proechimys cuvieri (left, AMNH 267029) and P. guyannensis (right, AMNH 267037). Tails of cuvieri are conspicuously hairier than those of guyannensis, an external difference that is useful for field identification of these sympatric congeners.

Fig. 80. Dorsal, ventral, and lateral views of skulls of Proechimys cuvieri (left, AMNH 266592) and P. guyannensis (right, AMNH 266595). All views approximately Χ1.5.