Frugivorous and animalivorous bats (Microchiroptera): dental and cranial adaptations

The most derived fruit-eating bats have small canines, wide palates and molars with a distinctive labial rim. Paracone and metacone have moved from a dilambdodont position in the middle of the tooth to the labial side of the tooth where they form the labial cutting edge. Along with the well-developed and close fitting labial cutting edges of the premolars and canines, this cutting edge skirts nearly the entire perimeter of the palate. The labial rim of the lower teeth fit inside the labial rim of the upper teeth like two cookie cutters nesting one inside the other. Frugivores have a greater allocation of tooth area at the anterior end of the toothrow, while animalivorous species have more at the posterior end of the toothrow. The area occupied by canines of predators of struggling prey is greater than that for bats that eat non-struggling prey like fruit. In addition, frugivores have wider palates than long while many carnivores have longer palates than wide. Omnivores appear to have a more equal allocation of space to more kinds of teeth, particularly the incisors and non-molariform premolars, on the toothrow than do frugivores or animalivores. The mechanical nature of different food items is discussed and the suggestion made that describing foods in terms of their texture may be more important in tooth design than whether they are fruit or insect or vertebrate.     

Canine teeth of bats (Microchiroptera): size, shape and role in crack propagation

Upper canines in microchiropteran bats show a variety of cross-sectional shapes. A consistent feature of all species studied here is that the tooth is edged and not simply round or oval. Prominent sharp edges are positioned in several directions but particularly antero-medially toward the incisors and posteriorly toward the premolars. These edges appear to direct the cracks made in food items to the incisors or to the premolars. A continuous cutting edge is apparent in the occlusal view of the palate running from tip of canine to the ectoloph of the molars. Size and shape analysis indicates that larger bats have slender, rather than stouter, canines for their height, a condition that may be attributable to the nature of the prey. Most bats take prey that have little hard substance imbedded within. The compromises in tooth shape may vary between that of a terrestrial predator with short, conical canines for processing endoskeletal prey to that of a small flying predator with long, slender, edged canines for capturing and processing exoskeletal prey. Unicuspid teeth and how they might function in food break-up have been overlooked to the literature; such a study could lead to an understanding of how more complex teeth function.     

Morphology and function of the shoulder joint of bats (Mammalia: Chiroptera)1

The shoulder joint of the Microchiroptera shows a remarkable morphological variation that has been studied in 20 individual bats from 15 species and 11 families. The basic morphology of the shoulder joint, with a globular humeral head and a corresponding glenoid cavity, is found in the Megachiroptera and, within the Microchiroptera, in the Rhinopomatidae. Besides this basic shoulder joint, there are two derived joint types: the derived and specialized shoulder joint with a single articular surface on the scapula and a more-or-less oblong humeral head, and the derived and specialized shoulder joint with secondary articular surfaces on the trochiter and on the dorsal aspect of the scapula. The first type of derived joint is most strikingly developed in the Mormoopidae and the Noctilionidae, the second one in the Vespertilionidae and the Molossidae. It is suggested that both types of derived shoulder joints have the functional significance of reducing the pronatory movements of the abducted forearm during the downstroke of the wing-beat cycle. This suggested function of the secondary shoulder joint is a new approach to understanding this very peculiar structure. In species with these specialized shoulder joints, the downstroke musculature is comparatively better developed and the M. serratus ant. post. div. comparatively less well developed. A hypothesis is offered to explain and combine the osteological and myological findings. Each of the derived types of shoulder joints has developed independently more than once through parallel evolution.     

Australian Oligo-Miocene Mystacinids (Microchiroptera): upper dentition, new taxa and divergence of New Zealand species

The upper dentition of two Australian early Miocene mystacinids, Icaropsparadox and I. aenae, from Riversleigh, Queensland, are described for the first time. Also recognised is a late Oligocene mystacinid from Lake Palankarinna, South Australia. The new fossils help refine understanding about the evolutionary history of mystacinids in Australia, including their temporal and geographical range, possible dietary and roosting habits, and likely separation time of New Zealand mystacinids.     

Sexual dimorphism of cranial suture complexity in wild sheep (Ovis orientalis)

Sutural complexity (the degree of interdigitation) of 13 cranial sutures was compared between male and female wild sheep ( Ovis orientalis ) to investigate a morphological feature that is potentially important with respect to stress transmission in the skulls of males during fighting. Most facial sutures (four of six) were not sexually dimorphic, but two sutures, the maxillojugal and jugolacrimal, had greater complexity in males than in females, suggesting that significant forces may be transmitted through the facial region of rams, most likely during horn clashing. Most of the braincase sutures (five of seven) were more complex in males than in females, and different factors appear to underlie this sexual dimorphism. In females, increased complexity of sutures during ontogeny was predicted best by variables measuring growth of the skull, brain or face, while in males, changes in complexity were predicted best by variables representing mechanical loading and frontal bone growth.     

Geographic pattern of cranial differentiation in the Asian Midday Jird Meriones meridianus (Rodentia: Muridae: Gerbillinae) and its taxonomic implications

The existence of cryptic species in the midday jird (Meriones meridianus) has been suggested in literature, although based on little empirical data to support this hypothesis. In this study, a two‐dimensional landmark‐based geometric morphometric approach was used to investigate whether patterns in intraspecific variation in skull shape and size exist, using 110 skull specimens from more than 20 different localities along the distribution range of M. meridianus. This is the first study of morphological differences on such a big sample size and geographical range, and it tries to find whether skull shape variation in this species is best described as being clinal or rather reflecting cryptic diversity. The latter seems to be the case, as a dimorphic skull phenotype was found, reflecting a geographic disparity between the Middle East and the Far East specimens both in shape and in size. Distinct cranial differences were found in the overall cranial size and, also at the level of the inflation of the bulla, the elongation of the nasal, the length of the teeth row and the incisive foramen, as well as the distance in between the latter two. It thus seems that M. meridianus from Middle East is morphologically distinct from that of the Far East. Furthermore, our results also demonstrate that clinal variation could explain variation within Middle East populations, whereas a more heterogenous pattern is found for those of the Far East. The hypothesis that the observed phenotypic variation may reflect cryptic species is discussed, with the recommendation for a thorough taxonomical revision of the genus in the region.     

Extremely low threshold for photic entrainment of circadian activity rhythms in molossid bats (Molossus molossus; Chiroptera – Molossidae)

Circadian rhythms usually deviate from 24 h and must be synchronized (entrained) to the outer 24 h day by certain environmental periodicities called Zeitgebers. For almost all organisms the most efficient Zeitgeber is the light-dark cycle (LD). In mammals the photic Zeitgeber cues are exclusively received via retinal photoreceptors. It is still in debate whether this circadian photoreception is mediated by rods, cones, and/or other retinal cells. From recent results in mouse mutants a circadian photoreception via non-rod/non-cone retinal receptors was deduced. However, earlier observations in bats indicating a very low threshold for photic entrainment imply that circadian photoreception may be mediated by rod-like receptors. In the present study the threshold for photic entrainment was determined in the neotropical mastiff bat Molossus molossus. Six test animals (3 m, 3 f) were kept isolated in recording cages situated in light-tight and sound-attenuating wooden boxes with a special lighting device on top. Under constant ambient temperature of 25 ± 1°C, relative humidity of 60 ± 5%, and an irregular ad libitum feeding schedule, the bats were exposed intermittantly for longer times to constant physiological darkness (LD-X) or 12:12 h light dark cycles with physiological darkness during the dark time (D) and varying low light-time illuminances (L). Half of the bats had an extremely low threshold for photic entrainment, about 10⁻⁵ lux, while the other individuals’ free-running activity rhythm was entrained by LD cycles with 10⁻⁴, 10⁻² and 10⁻¹ lux in L. The illuminance of only 10⁻⁵ lux is the lowest threshold value for photic entrainment found thus far in vertebrates. Plausibility considerations suggest circadian photoreception via rod-like retinal receptors to be most probably involved in this case.     

Functional morphology of the stone canal in the sea urchin Eucidaris (Echinodermata: Echinoidea)

The lack of mesocoelomic pores and the existence of a stone canal connecting proto-and mesocoel are characteristic peculiarities of echinoderms in contrast with the situation in other trimeric archicoelomates. The ultrastructure of the stone canal has been studied in order to understand its function in the strategically important position between two coelomic spaces with different functions. The epithelium of the Eucidaris (Echinoidea) stone canal is composed of three cell types: (1) ciliated cells, (2) cells with long basal processes containing myofilaments, and (3) granulated cells, which may represent secretory neurons. Nerve fibres of two types are common in the epithelium. We consider the stone canal to be a structure controlling fluid transport; its wall may exert peristaltic movements or tonic contractions and dilations which are under control of the nervous system. The ciliated cells additionally may have phagocytotic capacities. Similarities with the fine structure of the wall of the mesocoelomic pores in the pterobranch Cephalodiscus are discussed.     

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.     

Reconstruction of the cranial musculature and masticatory function of the Pleistocene panamerican ground sloth Eremotherium laurillardi (Mammalia,Xenarthra, Megatheriidae)

Cranial musculature, dental function and mandibular movement patterns in Eremotherium laurillardi were reconstructed from the examination of crania and dentitions. Size, shape and pattern of muscle divisions were reconstructed from the examination of bony rugosities indicating muscle attachments. Details of masticatory muscle structure and function were based on dissections of the tree sloths Bradypus and Choloepus. Among sloths, masticatory muscles in E. laurillardi demonstrate a different synergist–antagonist pattern, reflecting greater emphasis on mediolateral mandibular movements. Eight cranial character complexes (anterior facial, zygomatic arch, superficial masseter, deep masseter–zygomaticomandibularis, pterygoid, temporal, occipital and occlusal) determined by interrelated contributions of each component made to group functions were identified. An elongate anterior face and predental spout in E. laurillardi allowed protrusion of a long narrow tongue at small degrees of gape, reflecting a probably ancestral xenarthran condition. Gape minimisation, in conjunction with the mediolaterally directed masticatory stroke in E. laurillardi, was a unique solution to increase masticatory efficiency by permitting molariform tooth shearing surfaces to remain in or near occlusion for a greater percentage of each chewing cycle.     

A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (chiroptera)

Bats (Order Chiroptera), the only mammals capable of powered flight and sophisticated laryngeal echolocation, represent one of the most species-rich and ubiquitous orders of mammals. However, phylogenetic relationships within this group are poorly resolved. A robust evolutionary tree of Chiroptera is essential for evaluating the phylogeny of echolocation within Chiroptera, as well as for understanding their biogeographical history. We generated 4 kb of sequence data from portions of four novel nuclear intron markers for multiple representatives of 17 of the 18 recognized extant bat families, as well as the putative bat family Miniopteridae. Three echolocation-call characters were examined by mapping them onto the combined topology: (1) high-duty cycle versus low-duty cycle, (2) high-intensity versus low-intensity call emission, and (3) oral versus nasal emission. Echolocation seems to be highly convergent, and the mapping of echolocation-call design onto our phylogeny does not appear to resolve the question of whether echolocation had a single or two origins. Fossil taxa may also provide insight into the evolution of bats; we therefore evaluate 195 morphological characters in light of our nuclear DNA phylogeny. All but 24 of the morphological characters were found to be homoplasious when mapped onto the supermatrix topology, while the remaining characters provided insufficient information to reconstruct the placement of the fossil bat taxa with respect to extant families. However, a morphological synapomorphy characterizing the Rhinolophoidea was identified and is suggestive of a separate origin of echolocation in this clade. Dispersal-Vicariance analysis together with a relaxed Bayesian clock were used to evaluate possible biogeographic scenarios that could account for the current distribution pattern of extant bat families. Africa was reconstructed as the center of origin of modern-day bat families.     

Geomorphometric differences among four species of Microtus in Turkey (Mammalia: Rodentia)

In order to determine the phenotypic associations of four morphologically similar species of Microtus occurring in Turkey, we applied landmark-based shape analysis. The skulls of Microtus anatolicus, M. dogramacii, M. guentheri and M. levis (= M. rossiaemeridionalis) were found to differ significantly in terms of both size and shape. M. guentheri had the biggest skull, while M. levis had the smallest. Sexual dimorphism was found in the shape of the skull in M. dogramacii and M. levis. The tympanic bulla area is enlarged in M. anatolicus compared to the other species. Mahalanobis distances (the distance between a point and the group mean, taking into account the within-group covariance-variance matrix) confirm the distinction of the arvalis group (M. levis) and socialis group (Microtus anatolicus, M. dogramacii, M. guentheri).     

Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins

Patterns of morphological variation play an important role in evolutionary diversification and are critical to an informed interpretation of interspecific differences. When patterns of genetic variation have not diverged substantially, it is possible to reconstruct the differences in selection which gave rise to morphological differences among extant species. Morphological variation patterns are compared between two tamarin species, the cotton-top tamarin (Saguinus oedipus) and the saddle-back tamarin (S. fuscicollis illigeri). Genetic, phenotypic, and environmental variance/covariance and correlation matrices were obtained for a series of 39 cranial characters in each species (cotton-top tamarin, N = 328; saddle-back tamarin, N = 209) and for the species combined using crania from individuals of known genealogical relationship. After accounting for the effects of estimation error on measures of matrix similarity, patterns of phenotypic, genetic, and environmental variation and correlation were found to be very similar across species and among the types of variance within species. Taking the saddle-back tamarins as the standard, cotton-top tamarins have been selected for an enlarged anterior temporalis attachment area and increased facial prognathism. In primates, an enlarged anterior temporalis muscle is associated with incisive food preparation, especially at wide gape.     

Morphology of the middle ear of golden moles (Chrysochloridae)

The middle ear structures of nine species of golden moles (family Chrysochloridae) were examined under the light microscope. Auditory structures of several of these species are described here for the first time in detail, the emphasis being on the ossicular apparatus. Confirming previous observations, some golden moles (e.g. Amblysomus species) have ossicles of a morphology typical of mammals, whereas others ( Chrysospalax , Chrysochloris , Cryptochloris and Eremitalpa species) have enormously hypertrophied mallei. Golden moles differ in the nature and extent of the interbullar connection, the shape of the tympanic membrane and that of the manubrium. The stapes has an unusual orientation, projecting dorsomedially from the incus. It has been proposed that hypertrophied ossicles in golden moles are adapted towards the detection of seismic vibrations. The functional morphology of the middle ear apparatus is reconsidered in this light, and it is proposed that adaptations towards low-frequency airborne hearing might have predisposed golden moles towards the evolution of seismic sensitivity through inertial bone conduction. The morphology of the middle ear apparatus sheds little light on the disputed ordinal position of the Chrysochloridae.     

Phylogenetics and biogeography of the broad-nosed bats, genus Platyrrhinus (Chiroptera: Phyllostomidae)

The Neotropical broad-nosed bats, genus Platyrrhinus, represent a well-defined monophyletic group of 14 recognized species. A recent study of morphological characters confirmed Platyrrhinus monophyly and species diagnosis, but offered little support to their intra-specific relationships. We conducted phylogenetic analyses of the genus, using dense taxonomic sampling in combination with four gene sequences representing both mitochondrial and nuclear DNA transmission systems. Our aim was to elucidate the phylogenetic structure among species, using the resulting 3341 bp of DNA. Maximum parsimony, maximum likelihood, and Bayesian inference analyses produced similar topologies that confirm the monophyly of the genus Platyrrhinus and strongly support many previously unrecognized groups. Paraphyly of Platyrrhinus helleri and the unclear position of P. brachycephalus in the clades were also apparent in the data. Our biogeographical analysis suggests a Brazilian Shield origin for Platyrrhinus, followed by subsequent radiations of lineages in the Amazon Basin and Andes. Secondary dispersal from Amazonian and Andean centers is responsible for the Platyrrhinus inhabiting the Guianan Shield and the Pacific lowlands and Central America, respectively.     

A tale of two siblings: multiple paternity in big brown bats (Eptesicus fuscus) demonstrated using microsatellite markers

In many bat species, the opportunity for sperm competition or other mechanisms of post-copulatory paternity biasing is thought to be great, due to the long delay between copulation and fertilization, demonstrated sperm storage capabilities, and observed promiscuity. We present the results of the first study to assess whether litters of big brown bats (Eptesicus fuscus) containing dizygotic twins share the same father. We sampled 26 mother-offspring triads from three colonies in Indiana and Illinois, as well as 299 additional adults (237 females and 62 males) from these colonies and six other maternity colonies in the same area in 1997-1998. All individuals were genotyped at nine highly variable autosomal microsatellite loci and one X-linked locus. We assessed multiple paternity using autosomal and X-linked locus exclusions, and using maximum-likelihood methods. All methods confirmed multiple paternity within litters, and the maximum-likelihood analyses indicated that almost half of the sampled litters were composed of maternal half-siblings rather than full-siblings. Our results highlight the potential importance of post-copulatory mechanisms of paternity determination in the mating system of big brown bats, and have important implications for gene flow and population structuring in this species.