Mark D. Engstrom

Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: implications for conservation

Fourteen species of bats are reported for the first time from Guyana (Saccopteryx gymnura, Micronycteris brachyotis, M. homezi, Lichonycteris obscura, Anoura latidens, Vampyressa pusilla, Vampyrodes caraccioli, Eptesicus chiriquinus, Cynomops paranus, Molossops neglectus, Molossus sp., Molossus coibensis, Molossus sinaloae, and Promops centralis) bringing the known bat diversity for the country to 121 species. Information including measurements, reproductive data, distribution, and taxonomy are provided for these species. Seven of these new records were collected in the Iwokrama International Rain Forest Programme site in central Guyana. Eighty-six bat species are now documented from Iwokrama Forest which is the highest species diversity for bats reported from any protected area in the world. There are, however, few tropical sites that have relatively complete inventories. A summary for bat species diversity in southern Venezuela, Guyana, Suriname, and French Guiana indicates that at least 146 species of bats are known from the Guianan subregion. Intense inventory surveys, especially in the often neglected subcanopy, suggest that species richness is probably underestimated in most Neotropical areas. Likewise, species-level diversity in the Guianan subregion is higher than previously suggested. Surveying and monitoring biodiversity are critical to developing a National Protected Areas System in Guyana.

Molecular Differentiation of Large Species of Fruit-Eating Bats (Artibeus) and Phylogenetic Relationships Based on the Cytochrome b Gene

We analyzed the phylogenetic relationships of all eleven currently recognized species of large Artibeus using the cytochrome b mitochondrial gene. The topology from a maximum parsimony analysis included: (1) A. obscurus and A. planirostris as sister species with successively basal lineages of (2) A. amplus, (3) a clade with A. lituratus and A. intermedius, (4) A. jamaicensis, (5) a clade of A. inopinatus sister to A. hirsutus and A. fraterculus, (6) A. fimbriatus, and (7) the most basal lineage of A. concolor. The individual species were monophyletic and well supported by bootstrap and decay values. The monophyletic clade of ((((obscurus + planirostris) + amplus) + (lituratus + intermedius)) + jamaicensis) was also highly supported, although some of the interspecific relationships were less so. Contrary to previous hypotheses of species limits based on a presumed intergradation in body size, A. jamaicensis and A. planirostris do not form a monophyletic group, refuting their conspecificity and supporting an earlier study concluding that these two taxa represent separate morphological populations. An analysis with A. jamaicensis and A. planirostris constrained as sister-taxa resulted in a tree 8 steps longer. In addition, the low genetic pair-wise difference between A. lituratus and A. intermedius (2.8% with Kimura-2 parameters) warrants closer examination of their species limits.

Bat community structure at Iwokrama Forest, Guyana

With 86 species, Iwokrama Forest in central Guyana has the highest reported bat biodiversity for a protected area in the world. Using standardized capture data for 73 of these 86 species, we document community structure of bats in terms of species diversity, relative abundance, gross biomass, feeding guilds, vertical stratification and a trophic-size niche matrix. Based on faunal surveys in 1997, with similar amounts of effort in the forest canopy and at ground level, the greater fruit-eating bat (Artibeus lituratus) was by far the most ecologically dominant species in terms of frequency of capture and biomass. In total, frugivores comprised 70% of the species diversity and 78% of the biomass. The most common species of bat were fully partitioned in a resource niche matrix of size and trophic guild when vertical stratification was included as a variable. We conclude that resource partitioning and species packing differentially affect relative size in tropical bats, and are better summarized and analysed in three dimensions.

Systematics of the genera Carollia and Rhinophylla based on the cytochrome-B gene

Intrageneric relationships within Carollia and Rhinophylla (Phyllostomidae) are examined using the 1,140 base pairs of the mitochondrial cytochrome-b gene. We also examined the proposed sister relationship of Carollia and Rhinophylla by comparing the cytochrome-b gene from those two taxa to that of representatives of Phyllonycteris, Lonchophylla, Uroderma, Artibeus, Dermanura, Enchisthenes, and Chiroderma. Within Carollia, representatives of C. brevicauda and C. perspicillata are most closely related, whereas C. subrufa is more closely related to these two species than is C. castanea, which forms the basal divergence for the genus. Within Rhinophylla, data for relationships of species are equivocal and suggest a concomitant divergence for all three species. If the rate of evolution is the same for the cytochrome-b gene in the two genera, then species within Rhinophylla diverged earlier than did any of the species of Carollia. If those two genera shared a common ancestor to the exclusion of the remainder of the Phyllostomidae, common ancestry was of short duration. The alternative hypothesis, that Carollia and Rhinophylla are not sister taxa and shared morphological characteristics are convergent, remains viable based on our data.

Mammals of Iwokrama Forest

Abstract As part of a larger project on biodiversity and conservation in Guyana, we documented 130 species of mammals from Iwokrama Forest. This included 7 marsupials, 4 xenarthrans, 86 bats, 5 primates, 8 carnivores, 1 perissodactyl, 4 artiodactyls, and 15 rodents. As is typical for most Neotropical sites, the 86 species of bats represent over half of the mammal diversity. Standardized collecting methods implemented in the 1997 faunal survey of Iwokrama Forest in central Guyana enabled us also to investigate species diversity and abundance resulting from the inventory of mammals. Four species of fruit-eating bats (Artibeus lituratus, A. obscurus, A. planirostris, and Carollia perspicillata) were the most abundant and accounted for 43% of the 2,097 total captures in mist nets and harp traps during 79 nights of sampling. For nonvolant mammals, terrestrial spiny rats (Proechimys spp.) represented over half (55%) of the 65 captures in primarily live box-style traps. We estimate that our inventory is approximately 70% complete with an additional 57 species of mammals expected to occur in Iwokrama Forest. More specialized field techniques are required to attain a complete inventory of mammals, and long-term monitoring should be established at several sites to study spatial and temporal variation.

SYSTEMATICS OF DOG-FACED BATS (CYNOMOPS) BASED ON MOLECULAR AND MORPHOMETRIC DATA

Abstract Cynomops (dog-faced bat) generally is regarded as either a monophyletic genus or, in some cases, a subgenus of Molossops. Species limits and phylogenetic relationships within Cynomops, however, remain unresolved due primarily to subtle morphological differences and similarity in size of the small taxa. We used a combination of morphometric analyses for quantifying size variation and molecular data for reconstructing the evolutionary history within Cynomops. Rooting the tree with Eumops hansae produced a clade of Molossops neglectus and M. temminckii that was sister to a monophyletic Cynomops clade. The most parsimonious topology (in parenthetical notation) for Cynomops was (((paranus + planirostris) + (greenhalli + abrasus)) + mexicanus). Molecular analysis supports the autapomorphy of white venter as diagnostic for C. planirostris, although there was some overlap in size with the slightly larger, dark-venter C. paranus. Cynomops greenhalli was intermediate in size between C. paranus and C. mexicanus, but molecular analyses placed it as sister to the large-sized C. abrasus. The western Mexico endemic C. mexicanus, traditionally considered a subspecies of C. greenhalli, averaged larger in size than the other small Cynomops taxa and was the most basal lineage, requiring its designation as a distinct species.

Vocal Stereotypy and Singing Behavior in Baiomyine Mice

Abstract We examined spectral features that characterize the highly stereotyped, repetitive vocalizations of New World baiomyine rodents. Although stereotyped vocal signaling, described as “song,” has been documented in Scotinomys (singing or brown mice), its occurrence was unknown in the sister taxon Baiomys (pygmy mice). We also recorded vocalizations of females, about which little information was previously available. Although examination of morphological and molecular data supports a close relationship between the 2 baiomyine genera, we identified song as a complex behavior that further underpins the monophyly of the Baiomyini. Both spectral and temporal features render these songs highly localizable, a characteristic of possible utility for courtship and other social behavior. The song of Baiomys is confined entirely to the ultrasonic spectrum, unlike that of Scotinomys, which uses a broader range of frequencies. The intensity, identity, and predictability of vocalization suggest that these songs are purposeful and carry information important for species identification.

A New Species of Peropteryx (Chiroptera: Emballonuridae) from Western Amazonia with Comments on Phylogenetic Relationships within the Genus

Abstract We report the discovery of a new species of doglike bat (Peropteryx) from the lowland Amazonian forests of Ecuador and Peru. It has transparent wing membranes that are faintly tinged brown with pale-brown arms and digits; ears that are separated on the forehead; and a skull with small, shallow pterygoid pits that are anterolateral to an undivided basisphenoid pit and that are separated by a mesopterygoid extension. These characters distinguish the new species from morphologically similar species with which it was previously confused (P. leucoptera and P. macrotis). A molecular phylogenetic analysis of unlinked loci from each of the four genetic transmission systems of mammals (mitochondrial, nuclear-autosomal, X, and Y chromosomes) independently corroborated the placement of the new species as the sister taxon to a clade that includes P. kappleri, P. macrotis, and P. trinitatis; the basal lineage for the genus is P. leucoptera. This phylogeny suggests that transparent wings (sometimes described as “white” but actually lacking pigment), the traditional character used to diagnose Peronymus, is not a unique synapomorphy. Furthermore, based on a molecular dating analysis, the depth of divergence of Peropteryx is equivalent to that of another New World emballonurid genus (Balantiopteryx). Therefore, Peronymus does not warrant higher-level recognition as a subgenus or genus.

NEW SPECIES OF DISK-WINGED BAT THYROPTERA AND RANGE EXTENSION FOR T. DISCIFERA

Abstract A new species of disk-winged bat (Thyroptera) is described from the savannah habitats of the Cerrado in Brazil and Rupununi in Guyana. It is most similar to the primarily forest-dwelling T. lavali because of shared morphology, including oval-shaped disks on the thumbs as opposed to circular disks in the other species (T. tricolor and T. discifera). However, the new species has distinct countershading with dark brown dorsal fur that is in contrast to pale brown ventral fur with frosted tips. The other species have either white or yellowish brown ventral fur. During the examination of comparative material for this description, some older material that was faded in color and previously reported as T. tricolor was assigned to T. discifera, representing a range extension of more than 1,000 km to the east and the 1st documentation of T. discifera in the Atlantic Forest of Brazil.

Systematic review of small fruit-eating bats (Artibeus) from the Guianas, and a re-evaluation of A. glaucus bogotensis

Abstract We studied molecular and morphological variation in small fruit-eating bats (Artibeus) in northern South America to establish species boundaries, evolutionary relationships, and distributional limits. Although this is a speciose genus with some of the most common bats in Neotropical forests, resolution of taxonomy and their identification has been difficult. Our molecular phylogeny based on Bayesian and parsimony analyses of cytochrome b variation includes a well supported topology of A. glaucus glaucus sister to a clade of A. gnomus and A. glaucus bogotensis indicating that A. glaucus is a paraphyletic amalgam. A re-assessment of morphology corroborates differences between A. g. bogotensis from the Andean valleys of Colombia east into the Guianas and A. g. glaucus from western Amazonia. Thus, we recognize A. bogotensis and A. glaucus as distinct and allopatrically occurring species. Based on a Kimura-2 parameter model of substitution for cytochrome b, there was 1.2% sequence divergence within A. bogotensis, and 9.5% sequence divergence between A. bogotensis and A. glaucus. Compared to A. glaucus, A. bogotensis has prominent white facial stripes, a less hirsute interfemoral membrane, less robust orbitorostral region, and also lacks a small third lower molar. Within the Guiana region, there are three species with overlapping distributions (A. bogotensis, A. cinereus, and A. gnomus), however, they are sympatric only within the interior lowland forest near savannas. All other habitats including coastal forest, lowland forest, savanna, and highland forest have only two sympatric species, one of which is relatively more abundant (> 70%).