Nancy B. Simmons

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

A phylogenetic supertree of the bats (Mammalia: Chiroptera).

We present the first estimate of the phylogenetic relationships among all 916 extant and nine recently extinct species of bats (Mammalia: Chiroptera), a group that accounts for almost one‐quarter of extant mammalian diversity. This phylogeny was derived by combining 105 estimates of bat phylogenetic relationships published since 1970 using the supertree construction technique of Matrix Representation with Parsimony (MRP). Despite the explosive growth in the number of phylogenetic studies of bats since 1990, phylogenetic relationships in the order have been studied non‐randomly. For example, over one‐third of all bat systematic studies to date have focused on relationships within Phyllostomidae, whereas relationships within clades such as Kerivoulinae and Murinae have never been studied using cladistic methods. Resolution in the supertree similarly differs among clades: overall resolution is poor (46.4% of a fully bifurcating solution) but reaches 100% in some groups (e.g. relationships within Mormoopidae). The supertree analysis does not support a recent proposal that Microchiroptera is paraphyletic with respect to Megachiroptera, as the majority of source topologies support microbat monophyly. Although it is not a substitute for comprehensive phylogenetic analyses of primary molecular and morphological data, the bat supertree provides a useful tool for future phylogenetic comparative and macroevolutionary studies. Additionally, it identifies clades that have been little studied, highlights groups within which relationships are controversial, and like all phylogenetic studies, provides preliminary hypotheses that can form starting points for future phylogenetic studies of bats.

PHYLOGENY OF PHYLLOSTOMID BATS (MAMMALIA: CHIROPTERA): DATA FROM DIVERSE MORPHOLOGICAL SYSTEMS, SEX CHROMOSOMES, AND RESTRICTION SITES

Abstract Phyllostomidae is a large (> 140 species), diverse clade of Neotropical bats. Different species in this family feed on blood, insects, vertebrates, nectar, pollen, and fruits. We investigated phylogenetic relationships among all genera of phyllostomid bats and tested monophyly of several genera (e.g., Micronycteris, Mimon, Artibeus, Vampyressa) using 150 morphological, karyological, and molecular characters. Results of parsimony analyses of these combined data indicate that all traditionally recognized phyllostomid subfamilies are monophyletic and that most taxa that share feeding specializations form clades. These results largely agree with studies that have used a taxonomic congruence approach to evaluate karyological, immunological, and limited sets of morphological characters, although our finding that Phyllostominae is monophyletic is novel. Our results indicate that several genera (Micronycteris, Artibeus, and Vampyressa) are not monophyletic. We propose a new classification for Phyllostomidae that better reflects hypothesized evolutionary relationships. Important features of this new classification include: (1) formal recognition of two clades that group nectarivorous and frugivorous subfamilies, respectively, (2) redefinition of Glossophaginae and recognition of two tribal-level taxa within that subfamily, (3) recognition of several tribal-level taxa in Phyllostominae, (4) formal recognition of two clades that have been colloquially referred to as “short-faced” and “long-faced” stenodermatines, (5) elevation of the subgenera of Micronycteris to generic rank, (6) recognition of Mesophylla as a junior synonym of Ectophylla, (7) recognition of Enchisthenes as a distinct genus, and (8) retention of Dermanura and Koopmania as subgenera of Artibeus. Although Vampyressa is not monophyletic in our tree, we recommend no nomenclatural change because we did not include all Vampyressa species in our study. Comparisons of character and taxonomic congruence approaches indicate that character congruence provides improved resolution of relationships among phyllostomids. Many data sets are informative only at limited hierarchical levels or in certain portions of the phyllostomid tree. Although both chromosomal and immunological data provide additional support for several clades that we identified, these data sets are incongruent with many aspects of our phylogenetic results. These conflicts may be due to methodological constraints associated with the use of karyological and immunological data (e.g., problems with assessing homologies and distinguishing primitive from derived traits). Among other observations, we find that Macrotus waterhousii, which has been thought to have the primitive karyotype for the family, nests well within the phyllostomine clade. This suggests that results of previous analyses of chromosomal data may need to be reevaluated. Mapping characters and behaviors on our phylogenetic tree provides a context for evaluating hypotheses of evolution in Phyllostomidae. Although previous studies of uterine evolution in phyllostomids and other mammals have generally supported the unidirectional progressive fusion hypothesis, our results indicate that intermediate stages of external uterine fusion are often derived relative to the fully simplex condition, and that reversals also occur with respect to internal uterine fusion. Uterine fusion therefore appears to be neither completely unidirectional nor progressive in Phyllostomidae. Evolution of the vibrissae and noseleaf is similarly complex and homoplasy is common in these structures; however, many transformations in these systems diagnose clades of phyllostomids. Within Phyllostomidae, there is considerable derived reduction in numbers of vibrissae present in various vibrissal clusters. The phyllostomid noseleaf seems to have become a much more elaborate and complex structure over evolutionary time. Primitively within the family, the spear was short, the internarial region was flat, and the horseshoe was undifferentiated from the upper lip. Subsequently, within the various subfamilies, the spear became more elongate, the central rib and other internarial structures evolved, and the labial horseshoe became flaplike or cupped in some taxa. Dietary evolution in phyllostomids appears somewhat more complex than previously thought. We find that most of the major dietary guilds (e.g., frugivory, sanguivory) are represented by a single large clade within Phyllostomidae, indicating that each feeding specialization evolved once. However, reversals do occur (e.g., loss of nectar- and pollen-feeding in many phyllostomines and stenodermatines), and some specializations may have evolved more than once (e.g., carnivory).

Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation

Bats (Chiroptera) represent one of the largest and most diverse radiations of mammals, accounting for one-fifth of extant species. Although recent studies unambiguously support bat monophyly and consensus is rapidly emerging about evolutionary relationships among extant lineages, the fossil record of bats extends over 50 million years, and early evolution of the group remains poorly understood. Here we describe a new bat from the Early Eocene Green River Formation of Wyoming, USA, with features that are more primitive than seen in any previously known bat. The evolutionary pathways that led to flapping flight and echolocation in bats have been in dispute, and until now fossils have been of limited use in documenting transitions involved in this marked change in lifestyle. Phylogenetically informed comparisons of the new taxon with other bats and non-flying mammals reveal that critical morphological and functional changes evolved incrementally. Forelimb anatomy indicates that the new bat was capable of powered flight like other Eocene bats, but ear morphology suggests that it lacked their echolocation abilities, supporting a ‘flight first’ hypothesis for chiropteran evolution. The shape of the wings suggests that an undulating gliding–fluttering flight style may be primitive for bats, and the presence of a long calcar indicates that a broad tail membrane evolved early in Chiroptera, probably functioning as an additional airfoil rather than as a prey-capture device. Limb proportions and retention of claws on all digits indicate that the new bat may have been an agile climber that employed quadrupedal locomotion and under-branch hanging behaviour.

Fossil Evidence and the Origin of Bats

The phylogenetic and geographic origins of bats (Chiroptera) remain unknown. The earliest confirmed records of bats date from the early Eocene (approximately 51 Ma) in North America with other early Eocene bat taxa also being represented from Europe, Africa, and Australia. Where known, skeletons of these early taxa indicate that many of the anatomical specializations characteristic of bats had already been achieved by the early Eocene, including forelimb and manus elongation in conjunction with structural changes in the pectoral skeleton, hind limb reorientation, and the presence of rudimentary echolocating abilities. By the middle Eocene, the diversification of bats was well underway with many modern families being represented among fossil forms. A new phylogenetic analysis indicates that several early fossil bats are consecutive sister taxa to the extant crown group (including megabats), and suggests a single origin for the order, at least by the late Paleocene. Although morphological studies have long placed bats in the Grandorder Archonta, (along with primates dermopterans, and tree shrews), recent molecular studies have refuted this hypothesis, instead strongly supporting placement of bats in Laurasiatheria. Primitively, proto-bats were likely insectivorous, under-branch hangers and elementary gliders that exploited terminal branch habitats. Recent work has indicated that a number of other mammalian groups began to exploit similar arboreal, terminal branch habitats in the Paleocene, including multituberculates, eulipotyphlans, dermopterans, and plesiadapiforms. This may offer an ecological explanation for morphological convergences that led to the erroneous inclusion of bats within Archonta: ancestral archontan groups as well as proto-bats apparently were exploiting similar arboreal habitats, which may have led to concurrent development of homoplasic morphological attributes.

On the Cranial Osteology of Chiroptera. I. Pteropus (Megachiroptera: Pteropodidae)

Abstract Although detailed anatomical descriptions of skull morphology are available for representatives of many mammalian orders, no such descriptive work exists for bats, a group that comprises over 20% of extant mammalian species. In this paper, we provide a detailed description of the skull of Pteropus (Mammalia: Chiroptera: Megachiroptera: Pteropodidae) and establish a system of cranial nomenclature following the Nomina Anatomica Veterinaria. Based on a series of specimens of Pteropus lylei, we describe the skull as a whole and the morphology of external surfaces of 24 bones (7 rostral, 16 cranial, plus the mandible) and 17 teeth. We describe internal surfaces and additional bones of disarticulated skulls of Pteropus livingstonii and use material from the same species to describe the middle ear ossicles and the petrosal bone. We include a description of the hyoid apparatus and larynx based on Pteropus tonganus and a description of the deciduous dentition based on Pteropus hypomelanus. Using a sectioned fetus, we determine the content and homology of all cranial foramina present in the skull of Pteropus. We outline the ontogenetic changes from newborn pups to adults, considering changes in skull shape and the sequence of bone fusion and tooth eruption. Based on selected comparisons to other megabats, we discuss broad patterns of variation in general cranial shape, and interspecific variation in sutures, foramina, processes, and dentition. Overall, this work establishes a descriptive and nomenclatorial benchmark for chiropteran skull anatomy in line with similar works in other mammalian orders, with the aim of creating common ground for comparative, phylogenetic, and functional studies of the bat skull, including comparisons with other mammals.

A phylogeny of megachiropteran bats (Mammalia: Chiroptera: Pteropodidae) based on direct optimization analysis of one nuclear and four mitochondrial genes

The phylogeny of megachiropteran bats (Mammalia: Chiroptera: Pteropodidae) has been investigated using several different molecular datasets. These studies differed widely in taxonomic and locus sampling, and their results tended to lack resolution of internal nodes and were themselves largely incongruent. To address this, we assembled a data set of 5 loci (up to 3.5 kbp from 12S rDNA, 16S rDNA, tDNA‐valine, cytochrome b, and the nuclear gene c‐mos) for 43 species of megachiropterans and 6 microchiropteran outgroups. We analyzed these data with direct optimization under equal costs for substitutions and indels. We used POY in a parallel setting, and searches consisted of replicated swapping + refinements (ratcheting, tree fusing, and iterative pass optimization). Our results indicate that Megachiroptera and all recognized genera (including Pteropus) are monophyletic, and that Melonycteris is the sister group of the clade containing all the other genera. Clades previously proposed using molecular data, as well as many new and traditional groups, were well‐supported, and various sources suggest that the degree of conflict with morphological data may be considerably less marked than previously supposed. Analysis of individual loci suffer 70% loss in the number of compatible groups recovered across all analyses with respect to combined analyses. Our results indicate that, within Megachiroptera, nectarivory and cave‐dwelling originated several times, but echolocation (used for obstacle detection) evolved only once. Megachiropterans likely originated in SE Asia‐Melanesia, and colonized Africa at least four times.

Understanding phylogenetic incongruence: lessons from phyllostomid bats

All characters and trait systems in an organism share a common evolutionary history that can be estimated using phylogenetic methods. However, differential rates of change and the evolutionary mechanisms driving those rates result in pervasive phylogenetic conflict. These drivers need to be uncovered because mismatches between evolutionary processes and phylogenetic models can lead to high confidence in incorrect hypotheses. Incongruence between phylogenies derived from morphological versus molecular analyses, and between trees based on different subsets of molecular sequences has become pervasive as datasets have expanded rapidly in both characters and species. For more than a decade, evolutionary relationships among members of the New World bat family Phyllostomidae inferred from morphological and molecular data have been in conflict. Here, we develop and apply methods to minimize systematic biases, uncover the biological mechanisms underlying phylogenetic conflict, and outline data requirements for future phylogenomic and morphological data collection. We introduce new morphological data for phyllostomids and outgroups and expand previous molecular analyses to eliminate methodological sources of phylogenetic conflict such as taxonomic sampling, sparse character sampling, or use of different algorithms to estimate the phylogeny. We also evaluate the impact of biological sources of conflict: saturation in morphological changes and molecular substitutions, and other processes that result in incongruent trees, including convergent morphological and molecular evolution. Methodological sources of incongruence play some role in generating phylogenetic conflict, and are relatively easy to eliminate by matching taxa, collecting more characters, and applying the same algorithms to optimize phylogeny. The evolutionary patterns uncovered are consistent with multiple biological sources of conflict, including saturation in morphological and molecular changes, adaptive morphological convergence among nectar‐feeding lineages, and incongruent gene trees. Applying methods to account for nucleotide sequence saturation reduces, but does not completely eliminate, phylogenetic conflict. We ruled out paralogy, lateral gene transfer, and poor taxon sampling and outgroup choices among the processes leading to incongruent gene trees in phyllostomid bats. Uncovering and countering the possible effects of introgression and lineage sorting of ancestral polymorphism on gene trees will require great leaps in genomic and allelic sequencing in this species‐rich mammalian family. We also found evidence for adaptive molecular evolution leading to convergence in mitochondrial proteins among nectar‐feeding lineages. In conclusion, the biological processes that generate phylogenetic conflict are ubiquitous, and overcoming incongruence requires better models and more data than have been collected even in well‐studied organisms such as phyllostomid bats.

Conflict and congruence in a combined DNA–morphology analysis of megachiropteran bat relationships (Mammalia: Chiroptera: Pteropodidae)

The phylogeny of megabats (Mammalia: Chiroptera: Megachiroptera) has been addressed only on molecular grounds, as little effort has previously been made to describe the impressive morphological variation of the group in terms of phylogenetically informative characters. Here we provide a morphological matrix of 236 characters from the integument, dentition, cranial and post‐cranial skeleton, digestive apparatus and urogenital system. This data set covers most characters discussed previously in more restricted taxonomic contexts, as well a large number of new characters. Our aim was to generate a phylogenetic hypothesis for megabats based on a combined analysis of morphological characters and available gene sequence data from four mitochondrial and one nuclear loci. We used direct optimization under conventional equal costs, as well as under a cost ratio that maximizes homology when inapplicables (gaps) are present. Our results contradict the allegedly high level of conflict between the molecular and morphological partitions. We found that, although morphology alone recovered trees different and to some extent incompatible with those from previous molecular analyses, the combination of the two sources of evidence easily accommodated the morphological and molecular signals, yielding a resolved and relatively well‐supported phylogeny of Megachiroptera that is in reasonable agreement with the current morphology‐based taxonomy of the group. Overall congruence favored the maximization of homology by a narrow margin. In addition, partial analyses showed that implied weighting of morphology performed slightly better than equal weighting with respect to the combined analyses.

The Importance of Methods: Archontan Phylogeny and Cladistic Analysis of Morphological Data

Perusal of the recent systematic literature leaves the impression that cladistic methodology has contributed little to resolving the relationships between primates and other placental mammals. Despite numerous cladistic analyses, no viable consensus has yet been reached among workers studying morphology (e.g., Novacek and Wyss, 1986; Wible and Novacek, 1988; Pettigrew et al., 1989; Novacek, 1990; Dumont, 1992; Beard, 1993) or molecular data (e.g., Ammerman and Hillis, 1990, 1992; Baker et al., 1991a; Mindell et al., 1991; Adkins and Honeycutt, 1991; Bailey et al., 1992). Most workers agree that primate origins lie somewhere among “archontan” mammals (tree shrews, bats, gliding lemurs, extinct plesiadapiformes), but there is little agreement concerning relationships among these groups and monophyly of Archonta is still an open question (Fig. 1). If cladistic analysis is the powerful tool that we suppose, then why haven’t the relationships of primates been resolved? Part of the answer may lie in the different approaches and methods employed by workers using cladistic methods to address archontan relationships.