Skulls Of Bats Research Articles

HIGH FREQUENCY OF BATS IN THE DIET OF THE BARN OWL TYTO ALBA IN A LOWLAND DRY FOREST IN TOLIMA, COLOMBIA

The cosmopolitan distribution of the Barn Owl Tyto alba and its relatively well documented diet through the study of pellets have provided evidence of the broad diversity of prey it relies on. In most studies, both in tropical and temperate regions, rodents are its main prey, with other small mammals and vertebrates, and insects complementing its diet. Although bats have been recorded in the diet of T. alba at many localities, they seldom represent an important part of its diet. This study describes the diet of a small colony of T. alba from a mosaic of agricultural fields, pastures for cattle ranching and tropical dry forests in Tolima, central Colombia. Overall, we collected 516 pellets between 2016 and 2017 in a non-systematic manner, and recovered 335 skulls of rodents (67%), bats (29%), birds (3%) and shrews (1%), as well as invertebrate prey. The large proportion of bats in the diet of T. alba in this study is only matched by a few other studies, and further documents the wide range of prey included in the diet of this nocturnal raptor. This is one of the first studies on the diet of T. alba in tropical dry forests in Colombia and complements the existing data on its diet in the American tropics and worldwide.

Anatomical and Morphological Structure of the Skull of a Juvenile Specimen of Myotis myotis (Chiroptera: Vespertilionidae).

Few studies analyze the morphology and anatomy of the bat skull, and most of them are incomplete. Some of the difficulties stem from the fact that, in the representatives of the order Chiroptera, the interosseous sutures disappear by fusing together before active flight begins, which takes place over only a few months. This study presents a detailed morphological and anatomical description of the skull of a juvenile specimen of Myotis myotis (Borkhausen, 1797). Juvenile skulls are difficult to preserve and often incomplete. Previously inconsistent terminology related to bones, sutures, and other cranial structures was unified, which will provide insight on the distribution of each structure in both juvenile and adult specimens to be investigated. The description fill in the gaps in knowledge about the cranial structures of Myotis myotis and the representatives of the family Vespertilionidae. This will allow for precise descriptions of the skulls of bats.

3D models related to the publication: A 50-million-year-old, three-dimensionally preserved bat skull supports an early origin for modern echolocation

3D models related to the publication: A 50-million-year-old, three-dimensionally preserved bat skull supports an early origin for modern echolocation

A 50-million-year-old, three-dimensionally preserved bat skull supports an early origin for modern echolocation

Bats are among the most recognizable, numerous, and widespread of all mammals. But much of their fossil record is missing, and bat origins remain poorly understood, as do the relationships of early to modern bats. Here, we describe a new early Eocene bat that helps bridge the gap between archaic stem bats and the hyperdiverse modern bat radiation of more than 1,460 living species. Recovered from ∼50 million-year-old cave sediments in the Quercy Phosphorites of southwestern France, Vielasia sigei's remains include a near-complete, three-dimensionally preserved skull-the oldest uncrushed bat cranium yet found. Phylogenetic analyses of a 2,665 craniodental character matrix, with and without 36.8 kb of DNA sequence data, place Vielasia outside modern bats, with total evidence tip-dating placing it sister to the crown clade. Vielasia retains the archaic dentition and skeletal features typical of early Eocene bats, but its inner ear shows specializations found in modern echolocating bats. These features, which include a petrosal only loosely attached to the basicranium, an expanded cochlea representing ∼25% basicranial width, and a long basilar membrane, collectively suggest that the kind of laryngeal echolocation used by most modern bats predates the crown radiation. At least 23 individuals of V.sigei are preserved together in a limestone cave deposit, indicating that cave roosting behavior had evolved in bats by the end of the early Eocene; this period saw the beginning of significant global climate cooling that may have been an evolutionary driver for bats to first congregate in caves.

A New Record of Hypsugo pulveratus on Amami-Oshima Island, Japan and Comparison with H. alaschanicus

Three vespertilionid bats were captured from Amami-Oshima Island, and had an average forearm length of 35 mm and average body weight of 8 g. From the side of the bat skulls, the ridge of the crown was slightly curved at the base of the snout; the second upper premolar (P2) in the bats was relatively large; the male baculum was shaped like an elongated, 3-mm-long spear tip and was very similar in both shape and size to that of Hypsugo pulveratus. The phylogenetic tree inferred from the mitochondrial COI gene sequences revealed that these bats clustered with H. pulveratus. Therefore, the bats from Amami-Oshima Island were identified as H. pulveratus. The present paper lists and depicts the morphological differences between H. pulveratus and H. alaschanicus so far known from the territory of Japan. Finally, genetic analysis based on the barcoding gene sequences revealed that these species formed distinct clades.

Functional correlates of skull shape in Chiroptera: feeding and echolocation adaptations.

Morphological, functional, and behavioral adaptations of bats are among the most diverse within mammals. A strong association between bat skull morphology and feeding behavior has been suggested previously. However, morphological variation related to other drivers of adaptation, in particular echolocation, remains understudied. We assessed variation in skull morphology with respect to ecology (diet and emission type) and function (bite force, masticatory muscles and echolocation characteristics) using geometric morphometrics and comparative methods. Our study suggests that variation in skull shape of 10 bat families is the result of adaptations to broad dietary categories and sound emission types (oral or nasal). Skull shape correlates with echolocation parameters only in a subsample of insectivorous species, possibly because they (almost) entirely rely on this sensory system for locating and capturing prey. Insectivores emitting low frequencies are characterized by a ventrally tilted rostrum, a trait not associated with feeding parameters. This result questions the validity of a trade-off between feeding and echolocation function. Our study advances understanding of the relationship between skull morphology and specific features of echolocation and suggests that evolutionary constraints due to echolocation may differ between different groups within the Chiroptera.

Sensory adaptations reshaped intrinsic factors underlying morphological diversification in bats

BackgroundMorphological evolution may be impacted by both intrinsic (developmental, constructional, physiological) and extrinsic (ecological opportunity and release) factors, but can intrinsic factors be altered by adaptive evolution and, if so, do they constrain or facilitate the subsequent diversification of biological form? Bats underwent deep adaptive divergences in skull shape as they evolved different sensory modes; here we investigate the potential impact of this process on two intrinsic factors that underlie morphological variation across organisms, allometry, and modularity.ResultsWe use comparative phylogenetic and morphometric approaches to examine patterns of evolutionary allometry and modularity across a 3D geometric morphometric dataset spanning all major bat clades. We show that allometric relationships diverge between echolocators and visually oriented non-echolocators and that the evolution of nasal echolocation reshaped the modularity of the bat cranium.ConclusionsShifts in allometry and modularity may have significant consequences on the diversification of anatomical structures, as observed in the bat skull.

Correlation of skull morphology and bite force in a bird-eating bat (Ia io; Vespertilionidae)

BackgroundGenetic and ecological factors influence morphology, and morphology is compatible with function. The morphology and bite performance of skulls of bats show a number of characteristic feeding adaptations. The great evening bat, Ia io (Thomas, 1902), eats both insects and birds (Thabah et al. J Mammal 88: 728-735, 2007), and as such, it is considered to represent a case of dietary niche expansion from insects to birds. How the skull morphology or bite force in I. io are related to the expanded diet (that is, birds) remains unknown. We used three-dimensional (3D) geometry of the skulls and measurements of bite force and diets from I. io and 13 other species of sympatric or closely related bat species to investigate the characteristics and the correlation of skull morphology and bite force to diets.ResultsSignificant differences in skull morphology and bite force among species and diets were observed in this study. Similar to the carnivorous bats, bird-eaters (I. io) differed significantly from insectivorous bats; I. io had a larger skull size, taller crania, wider zygomatic arches, shorter but robust mandibles, and larger bite force than the insectivores. The skull morphology of bats was significantly associated with bite force whether controlling for phylogeny or not, but no significant correlations were found between diets and the skulls, or between diets and residual bite force, after controlling for phylogeny.ConclusionsThese results indicated that skull morphology was independent of diet, and phylogeny had a greater impact on skull morphology than diet in these species. The changes in skull size and morphology have led to variation in bite force, and finally different bat species feeding on different foods. In conclusion, I. io has a larger skull size, robust mandibles, shortened dentitions, longer coronoid processes, expanded angular processes, low condyles, and taller cranial sagittal crests, and wider zygomatic arches that provide this species with mechanical advantages; their greater bite force may help them use larger and hard-bodied birds as a dietary component.

3D Photogrammetry of Bat Skulls: Perspectives for Macro-evolutionary Analyses

Photogrammetry (PH) is relatively cheap, easy to use, flexible and portable but its power and limitations have not been fully explored for studies of small animals. Here we assessed the accuracy of PH for the reconstruction of 3D digital models of bat skulls by evaluating its potential for evolutionary morphology studies at interspecific (19 species) level. Its reliability was assessed against the performance of micro CT scan (µCT) and laser scan techniques (LS). We used 3D geometric morphometrics and comparative methods to quantify the amount of size and shape variation due to the scanning technique and assess the strength of the biological signal in relation to both the technique error and phylogenetic uncertainty. We found only minor variation among techniques. Levels of random error (repeatability and procrustes variance) were similar in all techniques and no systematic error was observed (as evidenced from principal component analysis). Similar levels of phylogenetic signal, allometries and correlations with ecological variables (frequency of maximum energy and bite force) were detected among techniques. Phylogenetic uncertainty interacted with technique error but without affecting the biological conclusions driven by the evolutionary analyses. Our study confirms the accuracy of PH for the reconstruction of challenging specimens. These results encourage the use of PH as a reliable and highly accessible tool for the study of macro evolutionary processes of small mammals.

Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats

Morphological diversity may arise rapidly as a result of adaptation to novel ecological opportunities, but early bursts of trait evolution are rarely observed. Rather, models of discrete shifts between adaptive zones may better explain macroevolutionary dynamics across radiations. To investigate which of these processes underlie exceptional levels of morphological diversity during ecological diversification, we use modern phylogenetic tools and 3D geometric morphometric datasets to examine adaptive zone shifts in bat skull shape. Here we report that, while disparity was established early, bat skull evolution is best described by multiple adaptive zone shifts. Shifts are partially decoupled between the cranium and mandible, with cranial evolution more strongly driven by echolocation than diet. Phyllostomidae, a trophic adaptive radiation, exhibits more adaptive zone shifts than all other families combined. This pattern was potentially driven by ecological opportunity and facilitated by a shift to intermediate cranial shapes compared to oral-emitters and other nasal emitters.

Methods of biological maceration in the preparation of bat skulls: benefits and limitations

Osteologic collections are used as an aid to scientific and teaching activities, to provide information on specific vertebrate characteristics, such as body support, posture, mode of locomotion, feeding habits and ecological niche. Known techniques for cleaning entire skeletons or mammalian skulls vary according to the destination of the material, the objective of the study, the taxonomic group, and the size of the specimen. The objective of this study was to test three different methods of maceration for cleaning bat skulls (traditional biological maceration, controlled biological maceration using Dermestes maculatus and controlled biological maceration using necrophagous fly larvae). The methods were carried out during five consecutive months, and the minimum and maximum times taken by each method were recorded and documented. Cleaning by fly larvae was the least costly method; the whole process was carried out during the preparation of the osteologic material. The flies ovulated directly on the pieces and the time spent was relatively short. Cleaning by dermestid larvae also resulted in clean parts in a short period, however, its culture needs specific maintenance conditions, since the size of the colony oscillates according to environmental temperature.

Dietary Adaptations of the Feeding Apparatus in Bats

Diet evolution is considered a major driver of morphological differences and species diversification in mammals, but quantitative tests of morphological adaptation and diversification are scarce. Bats are an ideal system to investigate dietary adaptations; they represent 20% of all mammals, encompass nearly the full spectrum of mammal diets, and have highly diverse cranial morphologies and feeding behaviors. Here, we present research aimed at identifying whether and how the bat feeding apparatus has diversified in conjunction with diet evolution. We combine modern laboratory and field approaches to quantify and map the evolution of skull shape, muscle morphology, and feeding performance across major bat lineages. These methods include: Computed Tomography (CT) scanning and Diffusible Iodine Contrast Enhanced CT scanning, three‐dimensional biomechanical modeling, in vivo bite force measurements, and statistical tests of evolutionary adaptive regimes. With these detailed anatomical and performance datasets, we have been able to identify potential drivers and mechanisms of morphological and functional diversification of the bat feeding apparatus. Analyses of selective regimes indicate that the current diversity of bat skull shapes is best explained by adaptive evolution for both dietary and sensory demands, with striking differences among bats that use different forms of echolocation, or none at all, and among diet specialists. Species that specialize on different diets differ in skull size and shape and in the morphology of their jaw muscles, including physiological cross‐sectional areas, origin and insertion areas, and fiber architecture. Importantly, our biomechanical models indicate that these morphological differences translate into differences in feeding performance metrics that are relevant to food processing, including maximum bite force and gape. For example, for their size, species with a foreshortened rostrum and large temporalis muscles are able to generate high bite forces at the expense of a wide gape, and this allows them to consume tough but relatively small food items. Altogether, these results illuminate the potential drivers and mechanisms of morphological and ecological diversification in bats, and possibly other mammals.Support or Funding InformationNational Science Foundation award 1557125This abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Feeding mechanisms in bats: variation within the constraints of flight

By any standard, bats are a successful group of mammals and the evolution of flight and echolocation were certainly key innovations behind their success. That is only part of the story, however. Bats have diversified into trophic niches that range from insectivory to feeding on blood, fruit, or nectar. While flight places fundamental constraints on the shape of the postcranial skeleton, skull shape in bats is remarkably diverse. Morphological studies of individual families and sympatric assemblages demonstrate that variation in skull shape is clearly associated with trophic specialization. Field experiments demonstrate that species-specific biting behaviors during feeding are common and analyses indicate that the evolution of cranial morphology and feeding behavior are correlated. Modeling experiments further suggest that feeding (loading) behaviors and skull shape are functionally linked. If the skulls of bats are under selective pressure for minimal mass because of the energetic demands of flight, then they may be more "optimized" to meet mechanical demands than are the skulls of other mammals. This would make bats a unique model system for studying the evolution of diversity in skull shape and its functional implications for the evolution of feeding strategies in mammals.

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

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.

Geometric morphometrics and cladistics: testing evolutionary relationships in mega- and microbats

Traditionally, morphometric data have consisted of distances, angles, or ratios, and have been considered inappropriate for cladistic analyses. Recently, geometric morphometrics, based on homologous landmark point-coordinates, has provided a number of advantages over traditional morphometric data and methods, including the possibility that phylogenetically informative characters and character-states may be extracted and used in cladistic analyses. Using two data sets of 3-dimensional point coordinates collected from skulls of bats, we empirically evaluate this possibility. Partial warps were extracted from the point-coordinate matrix, and these were then re-coded by gap-coding, for use in the cladistic analyses. In the case of samples from Eidolon helvum populations (two mainland localities and four islands in the Gulf of Guinea), analyzing males and females separately, our analyses based on these data were unable to detect consistent phylogeographic patterns among the populations. In the case of samples from plecotine bat species, these analyses produced a consensus cladogram showing considerable concordance with an earlier cladistic analysis by us of this group. In both cases, our results reflect those of earlier studies (based on both morphologic and genetic data), suggesting that the data and analytic techniques described herein may have interesting utility in cladistic analyses.

Finite‐element analysis of biting behavior and bone stress in the facial skeletons of bats

The wide range of dietary niches filled by modern mammals is reflected in morphological diversity of the feeding apparatus. Despite volumes of data on the biomechanics of feeding, the extent to which the shape of mammal skulls reflects stresses generated by feeding is still unknown. In addition to the feeding apparatus, the skull accommodates the structural needs of the sensory systems and brain. We turned to bats as a model system for separating optimization for masticatory loads from optimization for other functions. Because the energetic cost of flight increases with body mass, it is reasonable to suggest that bats have experienced selective pressure over evolutionary time to minimize mass. Therefore, the skulls of bats are likely to be optimized to meet functional demands. We investigate the hypothesis that there is a biomechanical link between biting style and craniofacial morphology by combining biting behavior and bite force data gathered in the field with finite-element (FE) analysis. Our FE experiments compared patterns of stress in the craniofacial skeletons within and between two species of bats (Artibeus jamaicensis and Cynopterus brachyotis) under routine and atypical loading conditions. For both species, routine loading produced low stresses in most of the skull. However, the skull of Artibeus was most resistant to loads applied via its typical biting style, suggesting a mechanical link between routine loading and skull form. The same was not true of Cynopterus, where factors other than feeding appear to have had a more significant impact on craniofacial morphology.

Patterns of Diversity in Cranial Shape Among Plant-Visiting Bats

Adaptations to a plant-based diet have evolved in bats on two occasions — once in the Old World family Pteropodidae and again within the New World family Phyllostomidae. Although the skulls of all plant-visiting bats exhibit adaptations for relatively large eyes, enlarged brains, and reduced molar complexity, the skulls of bats from the two families look very different. The goals of this study are to pinpoint the fundamental differences in the cranial shape between pteropodids and plant-visiting phyllostomids and to investigate patterns of diversity in cranial shape within each lineage. Analyses are based on 19 size adjusted, linear variables collected from 335 specimens that represent 71% of pteropodid and 45% of plant-visiting phyllostomid genera. Results of a stepwise discriminant function analysis indicate that differences in cranial shape between pteropodids and plant-visiting phyllostomids involve general aspects of relative braincase width, palate width and coronoid process height. Pteropodids have...

Analysis of Skull Measurements and Measurers: Can We Use Data Obtained by Various Observers?

To study sources of error in craniometric data and problems associated with using measurements taken by different observers, a sample of 10 bat skulls was measured with calipers three times by each of seven different individuals. Both intra- and inter-observer errors significantly contributed to the total variance of some characters. Intra-observer variability was responsible for -<17% of the total variance (median = 10%) whereas interobserver variability reached 30.7% (median = 3.9%). Characters with high intra-observer variability were those that exhibited high inter-observer variability. In comparisons involving measurements taken by different observers, a considerable risk exists that statistically significant results may arise due to measuring artifacts alone, especially when using large samples. However, measurements taken by different observers can be used in a single analysis if potentially risky characters are excluded from consideration. These include characters with high intra-observer variability, small means, or morphologically unclear endpoints.

The bats of Lord Howe Island with the description of a new Nyctophiline bat.

Bat specimens known from Lord Howe Island are discussed. Eptesicus pumilus was formerly a resident species but is now believed extinct. Published reports of Scotophilus morio are thought to refer to Eptesicus pumilus. A fossil bat skull found in a cave is described as a new species, Nyctophilus howensis. It may have occurred in modern times.

Tooth Development and Wear in Myotis

the end of the parturition period, it reveals the changes that occur in the deciduous dentition. The immature animals of the collection ranged in age from a few days to approximately 50 days (Stegeman, 1954). The deciduous teeth are shed during this period and the permanent dentition acquired. The number of specimens and the conditions under which they were obtained makes them meet most of the requirements set forth by Andersen (1918) for the determination of age, namely: (1) All specimens collected at one time; (2) All specimens collected from the same area; (3) A large series; and (4) Animals separated by one year of age. Since the skulls of adults were collected on a single date they can be separated into yearly groups more readily. Methods. -After the specimens were weighed, measured, and sexed the heads were severed, with the fur and flesh left on, each wrapped in a small square of cheesecloth, and a numbered tag attached. They were then dried and stored for future study. Several attempts were made to cook and clean these skulls without success. They were too fragile and came apart during the cleaning operation. A group was then exposed to dermestid larvae with no better success, since the larvae ate bones and all, particularly the immature specimens. The group was next infected with the larvae of the common clothes moth Tineola bisselliella (Hum.). These larvae were so small that they did not destroy the bones. Random samples were examined at intervals until the specimens were sufficiently clean to determine the condition of the teeth. The loosened tissues and frass were then removed and the examinations made under a binocular dissecting microscope. The deciduous teeth of each immature animal were listed and the total number recorded. The skulls were then classified on the basis of the number of milk teeth present. The skulls of mature bats were examined for tooth wear and grouped