Robert S. Voss

THE MAMMALS OF PARACOU, FRENCH GUIANA: A NEOTROPICAL LOWLAND RAINFOREST FAUNA PART 2. NONVOLANT SPECIES

Abstract This report describes the results of nonvolant mammal inventory fieldwork at Paracou, a lowland rainforest locality in northern French Guiana, and concludes the faunal analysis introduced by our previous monograph on the bats of Paracou (Simmons and Voss, 1998). Working within a 3–km radius over the course of 202 sampling dates from 1991 to 1994, we recorded a total of 64 nonvolant species by conventional trapping, arboreal platform trapping, pitfall trapping, diurnal and nocturnal hunting, and interviews with local residents. Included in this total species count are 12 marsupials, 9 xenarthrans, 6 primates, 10 carnivores, 5 ungulates, and 22 rodents. Systematic research with nonvolant mammal specimens collected as voucher material resulted in the discovery of new taxa, documented range extensions of previously described species, and helped resolve many longstanding taxonomic problems: (1) Gracilinanus emiliae (Thomas), herein reported for the first time from French Guiana, is redescribed and its known geographic distribution documented; based on examination of type material and original descriptions, G. longicaudus Hershkovitz is considered a junior synonym of G. emiliae, but Marmosa agricolai Moojen is not. (2) A new genus is proposed for Gracilinanus kalinowskii Hershkovitz, a taxon previously known only from eastern Peru, in recognition of its trenchant morphological differences from all other known didelphimorph marsupials. (3) Marmosops parvidens (Tate) and M. pinheiroi (Pine), the latter originally described as a subspecies of the former, are distinct species that occur sympatrically at Paracou; based on examination of type material, other taxa hitherto synonymized with M. parvidens are also judged to be valid species, including M. juninensis (Tate) and M. bishopi (Pine). (4) Monodelphis brevicaudata (Erxleben), M. glirina (Wagner), and M. palliolata (Osgood) are all distinct species diagnosable by unique combinations of morphological traits; based on examined specimens, M. brevicaudata (with type locality emended herein as Kartabo, Guyana) appears to be endemic to the Guiana subregion of Amazonia and to include both bicolored and tricolored phenotypes; a neotype from Cayenne, French Guiana, is designated to fix the application of Viverra touan Shaw as the oldest available name for the tricolored form. (5) Saguinus midas (Linnaeus) and S. niger (E. Geoffroy), currently treated as synonyms or conspecific races, are unambiguously diagnosable species that do not appear to be sister taxa; a neotype is designated to conserve current usage of niger E. Geoffroy for the black-handed tamarin of southeastern Amazonia. (6) Two new small species of Neacomys are described from material collected at Paracou; their diagnostic attributes are documented by detailed comparisons with other like-sized congeners from northern South America. (7) Nectomys melanius Thomas is recognized as a species distinct from N. squamipes (Brants) and N. palmipes J. A. Allen and Chapman; however, N. parvipes Petter is not a valid taxon and is herein synonymized with N. melanius. (8) The diagnostic characters of Neusticomys oyapocki (Petter and Dubost), a species previously known only from the holotype, are reevaluated and illustrated from freshly collected material. (9) Oecomys auyantepui Tate and O. paricola (Thomas), previously treated as synonyms, are valid species distinguished by consistent cranial differences and occupy allopatric ranges north and south of the Amazon, respectively. (10) A critical examination of small Oecomys specimens from Paracou and other Guianan localities supports the conclusions of other investigators that O. rutilus Anthony and O. bicolor (Tomes) are unambiguously diagnosable species. (11) Oligoryzomys fulvescens (Saussure) and O. microtis (J. A. Allen), currently regarded as valid allopatric species occurring north and south of the Amazon, respectively, are difficult to diagnose unambiguously and may be conspecific; new information is provided about the hitherto ambiguous type locality of the latter taxon. (12) Rhipidomys nitela Thomas is reported from French Guiana for the first time and its previously unpublished diagnostic differences from other congeners are tabulated and discussed. (13) A lectotype is designated for Coendou melanurus (Wagner), and the species is redescribed based on all known specimens in North American and European museums; diagnostic differences between this species and C. insidiosus (Olfers) are illustrated for the first time. (14) A red-rumped agouti (Dasyprocta) is designated as the neotype of Mus aguti Linnaeus to preserve current usage of Dasyprocta prymnolopha (Wagler) for the black-rumped agouti. (15) The diagnostic differences between red and green acouchies (Myoprocta) are discussed and a neotype is designated for Cavia acouchy Erxleben to fix the application of that name to the red species; other nominal taxa of Myoprocta are identified as red or green acouchies based on examination of type material and original descriptions. (16) The diagnostic morphological traits of Proechimys cuvieri Petter and P. guyannensis (E. Geoffroy) are reevaluated and discussed based on character variation in topotypical (French Guianan) material. Analyses of our sampling results indicate that distinct sets of nonvolant species are effectively sampled by different inventory methods, and that increased sampling effort with any method generally results in more species. Although the rate of discovery of new species always decreases with increasing sample size, none of our graphs of species accumulation indicate that an asymptotic value was reached with any method. Instead, nonparametric statistical extrapolations suggest that the Paracou nonvolant mammal fauna consists of somewhere between 69 and 74 species; by implication, our nonvolant inventory is about 86–93% complete. Most missing species are probably marsupials and rodents, but one or two expected primate species might have been locally extirpated by hunters prior to our fieldwork. In terms of higher taxonomic composition, the Paracou nonvolant mammal fauna is typical of those found throughout the humid Neotropical lowlands. However, a quantitative analysis of nonvolant faunal similarity at the species level among 12 exemplar rainforest inventories first clusters the Paracou list with others from the Guiana subregion of Amazonia, next with lists from elsewhere in Amazonia, and lastly with Central American lists. Pairwise similarity values likewise show an obvious positive correlation between faunal resemblance and geographic proximity within the Neotropical rainforest biome. At least 24 species (38%) of the Paracou nonvolant fauna are Amazonian endemics, but 18 (28%) are essentially pan-Neotropical in distribution; the remaining 22 species exhibit a variety of distributional patterns that suggest past connections among different sets of currently disjunct rainforested regions. Species richness comparisons among nonvolant faunal inventories are complicated by a variety of familiar problems including inconsistent methodology, presence or absence of certain key habitats, and uneven sampling effort. A conservative interpretation of sampling results from La Selva (Costa Rica), Paracou, and Manu (Peru), however, suggests progressive increases in richness of about 23% from Central America to the Guianas, and of about the same amount from the Guianas to western Amazonia; over the entire gradient (Central America to western Amazonia), the net increase in observed richness is at least 50%. Whereas rodents are consistently the most diverse clade in all well-sampled nonvolant faunas, rankings of other orders by relative richness exhibit considerable site-to-site variation, at least some of which appears to reflect real geographic differences in taxonomic diversity rather than sampling artifacts. Nonvolant rainforest mammals are hard to classify into trophic guilds due to behavioral plasticity and incomplete knowledge of relevant natural history. Preliminary guild comparisons among three exemplar faunas, however, suggest that the Paracou nonvolant community is substantially less diverse in arboreal frugivores and more diverse in terrestrial animalivores than are nonvolant communities at some Central American and western Amazonian sites. Subsistence and recreational hunting has clearly affected local populations of some nonvolant mammals at Paracou; whereas popular game species (e.g., large primates) were seldom sighted, density compensation may explain high local densities of certain other taxa (e.g., Potus flavus and Cuniculus paca). Patterns of differential habitat use between closely related nonvolant species at Paracou were mostly observed within the terrestrial granivore/frugivore guild. Combining these results with those previously reported for the sympatric bat fauna, we recorded a total of 142 mammalian species at Paracou. By statistical extrapolation from our sampling data, the entire local community perhaps contains 155–168 species; because the known French Guianan rainforest mammal fauna contains at least 167 species for which suitable habitat is present in our study area, such estimates are plausible. By implication, our inventory is perhaps 85–92% complete overall. A synthesis of biogeographic information analyzed in this monograph and by Simmons and Voss (1998) suggests that faunal turnover with increasing geographic distance is much higher for nonvolant mammals than for bats, a necessary consequence of observed group differences in endemicity: whereas many nonvolant rainforest mammals have geographic ranges bounded by obvious topographic or habitat discontinuities (e.g., large rivers, xeromorphic vegetation), most rainforest bats are geographically widespread. Not surprisingly, most of the taxa that usefully define a Guianan center of mammalian endemism are nonvolant species. The geographic limits of Guianan endemism appear to be rem

Phylogenetic Relationships and Classification of Didelphid Marsupials, an Extant Radiation of New World Metatherian Mammals

Abstract This report summarizes a decade of morphological and molecular research on the phylogenetic relationships of didelphid marsupials (opossums), a substantially intact radiation of New World metatherian mammals. We review the comparative morphology of Recent opossums, emphasizing those anatomical systems from which taxonomically useful information is available for the majority of living genera and species, namely the integument, cranium, and dentition. Morphological similarities and differences among didelphids and other plesiomorphic marsupials (caenolestids, microbiotheriids, dasyurids, and peramelids) are also described. These observations, representing evolved differences in diverse functional-morphological systems, together with karyotypic information gleaned from the literature, provide the basis for coding 129 phylogenetic characters that we scored for 44 ingroup and seven outgroup taxa. Published information about the size, internal organization, chromosomal location, and physiological properties of five nuclear genes (BRCA1, DMP1, IRBP, RAG1, vWF) sequenced for this study suggest that these loci are unlinked, exist as single copies, are active in different tissues, and encode protein products with widely divergent functions. All of the sequenced fragments are long (>900 bp), free of ingroup alignment ambiguities, and translate to open reading frame. Nucleotide data from a total of 7320 aligned sites were obtained from 43 ingroup and seven outgroup taxa. Separate parsimony, likelihood, and Bayesian analyses of these six data partitions (morphology + karyotypes, five genes) resulted in highly congruent estimates of didelphid phylogeny with few examples of conflict among strongly supported nodes. Analyses of concatenated sequences and combined (nonmolecular + sequence) datasets effectively summarize all of the common signal recovered from separate analyses: a completely resolved ingroup phylogeny with high support statistics at most nodes. Remaining problems (not conclusively resolved in this study) include the position of the ingroup root and the relationships of three genera (Chacodelphys, Cryptonanus, Tlacuatzin) within their respective suprageneric clades. The history of didelphid classification is reviewed, and all previous systems are found to contain nonmonophyletic groups. A revised phylogenetic classification consistent with our analytic results includes the following higher taxa: Glironiinae (for Glironia), Caluromyinae (Caluromys and Caluromysiops), Hyladelphinae (Hyladelphys), Didelphinae (Marmosini, Metachirini, Didelphini, and Thylamyini), Marmosini (Marmosa, Monodelphis, and Tlacuatzin), Metachirini (Metachirus), Didelphini (Chironectes, Didelphis, Lutreolina, and Philander), and Thylamyini (Chacodelphys, Cryptonanus, Gracilinanus, Lestodelphys, Marmosops, and Thylamys). The probable relationships of several Neogene fossil genera are also discussed. To facilitate identifications, all Recent genera are redescribed, representative crania are illustrated, and a key is provided.

PHYLOGENETIC STUDIES ON DIDELPHID MARSUPIALS II. NONMOLECULAR DATA AND NEW IRBP SEQUENCES: SEPARATE AND COMBINED ANALYSES OF DIDELPHINE RELATIONSHIPS WITH DENSER TAXON SAMPLING

Abstract In order to test the results of a previous study of didelphid marsupial phylogeny based on IRBP nuclear gene sequences (Jansa and Voss, 2000. Phylogenetic studies on didelphid marsupials I. Introduction and preliminary results from nuclear IRBP gene sequences. Journal of Mammalian Evolution 7: 43–77), we surveyed external, cranial, dental, and karyotypic characters among a more densely taxon-sampled didelphine ingroup. Separate maximum-parsimony analyses of these nonmolecular data and of a new (taxon-dense) IRBP matrix yielded superficially dissimilar strict-consensus topologies. However, no didelphine clade that was even moderately well supported by either separate analysis was contradicted by any equivalently well-supported clade in the other. Instead, all examples of taxonomic incongruence involved weak nodal support from one or both datasets. A maximum-likelihood analysis of the IRBP data produced a consensus topology that was completely congruent with, although slightly more resolved than, the maximum-parsimony consensus. A combined (simultaneous) maximum-parsimony analysis of both datasets (nonmolecular + IRBP) produced a consensus topology that closely resembled the results of analyzing IRBP separately. Most of the didelphine relationships previously reported by Jansa and Voss (op. cit.) are supported by these analytic exercises, with some notable exceptions. The taxon currently known as Marmosa canescens is conspicuously divergent from congeneric species and variously clusters with three different groups (“other Marmosa” + Micoureus, Monodelphis, or higher didelphines [= clade H of Jansa and Voss, op. cit.] ) in several parsimony-equivalent resolutions of a fourfold basal polytomy in the IRBP and combined-data consensus topologies. Even without canescens, however, the genus Marmosa is not demonstrably monophyletic. The nomenclatural consequences of these results are discussed, and a new genus is described for “Marmosa” canescens. Future analyses should test the monophyly of other speciose didelphine genera, but new sources of character data will be needed to offset the loss of resolution and decreased nodal support that are often caused by denser taxon sampling.

Ten New Genera of Oryzomyine Rodents (Cricetidae: Sigmodontinae)

Abstract In order to achieve a monophyletic classification of oryzomyine rodents, 10 new genera are described for species or species groups previously referred to the polyphyletic genus Oryzomys. The following names are proposed: Aegialomys, n.gen. (for the “xanthaeolus group” of authors); Cerradomys, n.gen. (for the “subflavus group”); Eremoryzomys, n.gen. (for polius); Euryoryzomys, n.gen. (for the “nitidus group”); Hylaeamys, n.gen. (for the “megacephalus group”); Mindomys, n.gen. (for hammondi); Nephelomys, n.gen. (for the “albigularis group”); Oreoryzomys, n.gen. (for balneator); Sooretamys, n.gen. (for angouya); and Transandinomys, n.gen. (for bolivaris and talamancae). All of the new genera thus constituted are morphologically diagnosable and have distinct ecogeographic distributions. Pending revisionary work that is currently in progress by other researchers, six species belonging to the “alfaroi group” (herein construed as including alfaroi, chapmani, melanotis, rhabdops, rostratus, and saturatior) are provisionally referred to Handleyomys. As a result of these changes, the genus Oryzomys is restricted to the “palustris group” of authors, and the tribe Oryzomyini now comprises 28 genera.

On the contents of Gracilinanus gardner and creighton, 1989, with the description of a previously unrecognized clade of small didelphid marsupials

Abstract Five nominal species of small didelphid marsupials previously referred to Gracilinanus differ conspicuously from the type species (G. microtarsus) and from all of the other valid taxa that we recognize as members of that genus (G. aceramarcae, G. agilis, G. dryas, G. emiliae, G. marica). These anomalous forms can be distinguished morphologically from Gracilinanus (in the strict sense just defined) by lacking maxillary palatal vacuities, a secondary foramen ovale, and a rostral process of the premaxillae; in addition, P3 is taller than P2, and accessory cusps are often present on C1. A new genus, Cryptonanus, is described to contain these forms, all of which are provisionally recognized as valid species: C. agricolai, C. chacoensis, C. guahybae, C. ignitus, and C. unduaviensis. Separate and combined phylogenetic analyses of nonmolecular data and nuclear gene sequences suggest that Cryptonanus and Gracilinanus (sensu stricto) are reciprocally monophyletic and closely related, although they were not consistently recovered as sister taxa in any analysis. Available specimen records document that Cryptonanus is widely distributed in mostly unforested tropical, subtropical, and temperate biomes south of the Amazon River (from ca. 7°S in the Brazilian state of Ceará to ca. 34°S in the Argentinian province of Buenos Aires), but significant range extensions could be expected from pitfall trapping in extralimital savanna landscapes. Scant field data suggest that species of Cryptonanus may often be associated with wet or seasonally inundated grasslands, an unusual habitat for small didelphids.

Morphological evolution in muroid rodents. I, Conservative patterns of craniometric covariance and their ontogenetic basis in the neotropical genus Zygodontomys

Analyses of craniodental measurement data from 15 wild‐collected population samples of the Neotropical muroid rodent genus Zygodontomys reveal consistent patterns of relative variability and correlation that suggest a common latent structure. Eigenanalysis of each sample covariance matrix of logarithms yields a first principal component that accounts for a large fraction of the total variance. Variances of subsequent sample principal components are much smaller, and the results of bootstrap resampling together with asymptotic statistics suggest that characteristic roots of the covariance matrix after the first are seldom distinct. The coefficients of normalized first principal components are strikingly similar from sample to sample: inner products of these vectors reveal an average between‐sample correlation of 0.989, and the mean angle of divergence is only about eight degrees. Since first principal component coefficients identify the same contrasts among variables as comparisons of relative variability and correlation, we conclude that a single factor accounts for most of the common latent determination of these sample dispersions. Analyses of variance based on toothwear (a coarse index of age) and sex in the wild‐collected samples, and on known age and sex in a captive‐bred population, reveal that specimen scores on sample first principal components are age‐ and sex‐dependent; residual sample dispersion, however, is essentially unaffected by age, sex, or age × sex interaction. The sample first principal component therefore reflects the covariance among measured dimensions induced by general growth, and its coefficients are interpretable as exponents of postnatal growth allometry. Path‐analytic models that incorporate prior knowledge of the equivalent allometric effects of general growth within these samples can be used to decompose the between‐sample variance by factors corresponding to other ontogenetic mechanisms of form change. The genetic or environmental determinants of differences in sample mean phenotypes induced by such mechanisms, however, can be demonstrated only by experiment.

Adaptive Evolution of the Venom-Targeted vWF Protein in Opossums that Eat Pitvipers

The rapid evolution of venom toxin genes is often explained as the result of a biochemical arms race between venomous animals and their prey. However, it is not clear that an arms race analogy is appropriate in this context because there is no published evidence for rapid evolution in genes that might confer toxin resistance among routinely envenomed species. Here we report such evidence from an unusual predator-prey relationship between opossums (Marsupialia: Didelphidae) and pitvipers (Serpentes: Crotalinae). In particular, we found high ratios of replacement to silent substitutions in the gene encoding von Willebrand Factor (vWF), a venom-targeted hemostatic blood protein, in a clade of opossums known to eat pitvipers and to be resistant to their hemorrhagic venom. Observed amino-acid substitutions in venom-resistant opossums include changes in net charge and hydrophobicity that are hypothesized to weaken the bond between vWF and one of its toxic snake-venom ligands, the C-type lectin-like protein botrocetin. Our results provide the first example of rapid adaptive evolution in any venom-targeted molecule, and they support the notion that an evolutionary arms race might be driving the rapid evolution of snake venoms. However, in the arms race implied by our results, venomous snakes are prey, and their venom has a correspondingly defensive function in addition to its usual trophic role.

Molecular Systematics of Mouse Opossums (Didelphidae: Marmosa): Assessing Species Limits using Mitochondrial DNA Sequences, with Comments on Phylogenetic Relationships and Biogeography

Abstract The genus Marmosa contains 15 currently recognized species, of which nine are referred to the subgenus Marmosa, and six to the subgenus Micoureus. Recent revisionary research based on morphological data, however, suggests that the subgenus Marmosa is more diverse than the currently accepted taxonomy indicates. Herein we report phylogenetic analyses of sequence data from the mitochondrial cytochrome-b gene representing 12 of the 14 morphologically defined taxa recently treated as valid species of Marmosa (Marmosa) in the aforementioned revisionary work. These data provide a basis for testing the monophyly of morphologically defined taxa in the subgenus Marmosa, and they afford the first opportunity to assess phylogenetic relationships among the majority of species currently referred to the genus. Ten of 11 species of Marmosa (Marmosa) represented by multiple sequences in our analyses were recovered as monophyletic. In contrast, our samples of M. mexicana were recovered as two deeply divergent haplogroups that were not consistently associated as sister taxa. Among other results, our analyses support the recognition of M. isthmica and M. simonsi as species distinct from M. robinsoni, and the recognition of M. macrotarsus and M. waterhousei as species distinct from M. murina. The validity of three other species long recognized as distinct (M. rubra, M. tyleriana, and M. xerophila) is also clearly supported by our results. Although cytochrome-b sequence data are not consistently informative about interspecific relationships in this study, we found strong support for several clades, including (1) the subgenus Micoureus; (2) a group comprised of Marmosa macrotarsus, M. murina, M. tyleriana, and M. waterhousei; (3) a group comprised of M. robinsoni and M. xerophila; and (4) a group comprising all of the species in the subgenus Marmosa that occur north and west of the Andes (M. isthmica, M. mexicana, M. robinsoni, M. simonsi, M. xerophila, and M. zeledoni). Our discovery of the latter clade suggests that the Andes may have played a major role in the early diversification of this speciose radiation of small Neotropical marsupials.

Base-Compositional Heterogeneity in the RAG1 Locus among Didelphid Marsupials: Implications for Phylogenetic Inference and the Evolution of GC Content

Although theoretical studies have suggested that base-compositional heterogeneity can adversely affect phylogenetic reconstruction, only a few empirical examples of this phenomenon, mostly among ancient lineages (with divergence dates > 100 Mya), have been reported. In the course of our phylogenetic research on the New World marsupial family Didelphidae, we sequenced 2790 bp of the RAG1 exon from exemplar species of most extant genera. Phylogenetic analysis of these sequences recovered an anomalous node consisting of two clades previously shown to be distantly related based on analyses of other molecular data. These two clades show significantly increased GC content at RAG1 third codon positions, and the resulting convergence in base composition is strong enough to overwhelm phylogenetic signal from other genes (and morphology) in most analyses of concatenated datasets. This base-compositional convergence occurred relatively recently (over tens rather than hundreds of millions of years), and the affected gene region is still in a state of evolutionary disequilibrium. Both mutation rate and substitution rate are higher in GC-rich didelphid taxa, observations consistent with RAG1 sequences having experienced a higher rate of recombination in the convergent lineages.

Species Limits and Phylogenetic Relationships in the Didelphid Marsupial Genus Thylamys Based on Mitochondrial DNA Sequences and Morphology

Abstract Species of the didelphid marsupial genus Thylamys, commonly known as fat-tailed mouse opossums, are broadly distributed in the open habitats of central and southern South America. In this report we examine species limits in the genus and infer phylogenetic relationships among Thylamys species using both molecular phylogenetic and morphological methods. We assessed species limits using a broad geographic sample of DNA sequences from the mitochondrial gene cytochrome b in conjunction with morphological character analysis, and we inferred phylogenetic relationships among species using the cytochrome-b dataset in addition to sequences from the mitochondrial genes cytochrome c oxidase subunit II and NADH dehydrogenase 2 for a representative subset of individuals. Based on the results of these analyses, we recognize Xerodelphys (new subgenus) for T. karimii and T. velutinus, and we recognize seven valid species in the nominotypical subgenus. The latter includes T. macrurus, T. pusillus, and two monophyletic species groups: the Elegans Group (T. elegans, T. pallidior, T. tatei) and the Venustus Group (T. sponsorius, T. venustus). Analysis of cytochrome-b sequences additionally reveals deep phylogeographic structuring in three species (T. pallidior, T. pusillus, T. venustus), each of which contains two or three robustly supported allopatric haplogroups. The existence of undescribed Peruvian forms of the Elegans Group is also plausibly indicated. We provide morphological diagnoses of all species recognized as valid in this report, summarize information about geographic distributions, comment on previous misidentifications, and briefly consider historical-biogeographic scenarios with a focus on dispersal events across the Andes.