Megachiropteran Bats Research Articles

Roost Preference in Three Species of Pteropodid Bats in Tirunelveli and Tenkasi, Tamilnadu, South India

Roost preference, roosting ecology and roost resource partitioning of megachiropteran bats in the plains of Tirunelveli and Tenkasi districts of Tamilnadu, South India, were investigated from January 2021 to December 2022. Three species of megachiropterans bats namely Pteropus medius, Cynopterus sphinx and Rosettus leschanaulti were recorded in the study area. P. medius roosts in open foliage on trees like Terminalia arjuna (46.90%), Samanea saman (13.53%), Ficus religiosa (12.09%), Ficus benghalensis (5.27%), Bassia latifolia (5.04%), Tamarindus indica (4.89%), Sygium cumini (4.71%), Manjifera Indica (2.32%), Thespesia populnea (1.93%), Pongamia pinnata (1.38%), Pithecellobium dulce (0.90%), Albizia lebbeck (0.74%), and Azadirachta indica (0.23%). C. sphinx roosts in Borassus flabellifer (68.55%), Polyalthia longifolia (25.90%) and Pritchardia pacifica (5.54%). Generally, the native trees are preferred by these bats as the favorite roost. R. leschanaulti prefers temples (56.52%), water wells (18.53%), stone buildings (17.16%) and abandoned houses (7.78%). Diversity measures with regard to Margalef index, Berger Parker index and Evenness index, comparatively; higher values were reported in C. sphinx (9.433), R. leschanaulti (0.270) and C. sphinx (0.925) respectively. The distribution pattern and roost preference of megachiropteran bats reveal that these bat species serve as bio-indicator of the agricultural landscape in the wetland ecosystem. It is evident that these three symbiotic bat species exhibit roost preference, and roost resources partitioning in the study area.

Ocular morphology of the fruit bat, Eidolon helvum, and the optical role of the choroidal papillae in the megachiropteran eye: a novel insight

This work was designed to provide a morphologic, morphometric and histochemical description of the eye of the African straw-coloured fruit bat (Eidolon helvum). An explanation of the optical role of the choroidal papillae in the vision of megachiropteran bats was provided. Enucleated eyes of captured fruit bats were measured and processed for light microscopy. Typical gross features of the mammalian eye including an anterior transparent cornea, posterior whitish sclera and a golden-brown iris surrounding a round pupil were observed in the eye. Presence of undulating retina typically found in megachiropterans was also seen. The ratio of mean corneal diameter to mean axial eye diameter was 0.58 ± 0.08. The histochemical investigation of the eye indicated the presence of mucins, proteoglycans, hyaluronic acid, glycogen and/or glycoproteins in the corneal, scleral, choroidal and retinal tissues. The presence of reflective materials of the tapetum lucidum on the undulating retina was shown to be a morphological adaptation for increased light sensitivity as each parabolic surface of the choroidal papillae served as a convex mirror, reflecting the light rays to the adjacent parabolic surface, thus sensitising photoreceptors in affected regions. This phenomenon thus empowers megachiropteran bats with improved scotopic visual capability and could explain why most of them are reliant on their vison without the need for echolocation.

The Mammalian Locus Coeruleus Complex-Consistencies and Variances in Nuclear Organization.

Descriptions of the nuclear parcellation of the locus coeruleus complex have been provided in approximately 80 mammal species spanning the phylogenetic breadth of this class. Within the mammalian rostral hindbrain, noradrenergic neurons (revealed with tyrosine hydroxylase and dopamine-ß-hydroxylase immunohistochemistry) have been observed within the periventricular grey matter (A4 and A6 nuclei) and parvicellular reticular nucleus (A5 and A7 nuclei), with the one exception to date being the tree pangolin, where no A4/A6 neurons are observed. The alphanumeric nomenclature system, developed in laboratory rodent brains, has been adapted to cover the variation observed across species. Cross-species homology is observed regarding the nuclear organization of noradrenergic neurons located in the parvicellular reticular nucleus (A5 and A7). In contrast, significant variations are observed in the organization of the A6 neurons of the locus coeruleus proper. In most mammals, the A6 is comprised of a moderate density of neurons, but in Murid rodents, primates, and megachiropteran bats, the A6 exhibits a very high density of neurons. In primates and megachiropterans, there is an additional moderate density of A6 neurons located rostromedial to the high-density portion. These variations are of importance in understanding the translation of findings in laboratory rodents to humans.

Nuclear organization of catecholaminergic neurons in the brains of a lar gibbon and a chimpanzee.

Using tyrosine hydroxylase immunohistochemistry, we describe the nuclear parcellation of the catecholaminergic system in the brains of a lar gibbon (Hylobates lar) and a chimpanzee (Pan troglodytes). The parcellation of catecholaminergic nuclei in the brains of both apes is virtually identical to that observed in humans and shows very strong similarities to that observed in mammals more generally, particularly other primates. Specific variations of this system in the apes studied include an unusual high-density cluster of A10dc neurons, an enlarged retrorubral nucleus (A8), and an expanded distribution of the neurons forming the dorsolateral division of the locus coeruleus (A4). The additional A10dc neurons may improve dopaminergic modulation of the extended amygdala, the enlarged A8 nucleus may be related to the increased use of communicative facial expressions in the hominoids compared to other primates, while the expansion of the A4 nucleus appears to be related to accelerated evolution of the cerebellum in the hominoids compared to other primates. In addition, we report the presence of a compact division of the locus coeruleus proper (A6c), as seen in other primates, that is not present in other mammals apart from megachiropteran bats. The presence of this nucleus in primates and megachiropteran bats may reflect homology or homoplasy, depending on the evolutionary scenario adopted. The fact that the complement of homologous catecholaminergic nuclei is mostly consistent across mammals, including primates, is advantageous for the selection of model animals for the study of specific dysfunctions of the catecholaminergic system in humans.

The detection of Japanese encephalitis virus in Megachiropteran bats in West Kalimantan, Indonesia: A potential enzootic transmission pattern in the absence of pig holdings

The West Kalimantan province in Borneo island, Indonesia belongs to endemic area of Japanese encephalitis (JE) that accounts for approximately 30% of total cases yearly. As the presence of pig holdings is uncommon in West Kalimantan, another reservoir host might have played a role in the local transmission of JE virus in this area. Current study aimed to identify the potential role of bats in the local transmission of JE by performing molecular detection of JE virus in bats and mosquitoes using RT-PCR. Sample collection was performed in 3 districts in West Kalimantan, covering 3 different ecosystems: forest, coastal, and residential areas. Bat collection was performed using mist net and harp net, while mosquito collection was carried out using animal-baited trap and human landing collection. A total of 373 blood samples from bats were tested for JE virus, among which 21 samples (5.6%) showed positive results, mainly from Cynopterus brachyotis (lesser short-nosed fruit bat) found in residential areas. Out of 53 mosquito pools, 3 JE-positive pools of Culex tritaeniorhynchus and Cx. vishnui were collected at the same location as JE-positive bats. Current study showed the first evidence of JE virus detection in several species of Megachiropteran bats in Indonesia, demonstrated the potential role of frugivorous bats in local transmission of JE in West Kalimantan. More aggressive measures are required in JE risk mitigation, particularly in initiating JE vaccination campaign and in avoiding disruption of bats’ natural habitats through changes in land-use.

Distribution, number, and certain neurochemical identities of infracortical white matter neurons in the brains of three megachiropteran bat species.

A large population of infracortical white matter neurons, or white matter interstitial cells (WMICs), are found within the subcortical white matter of the mammalian telencephalon. We examined WMICs in three species of megachiropterans, Megaloglossus woermanni, Casinycteris argynnis, and Rousettus aegyptiacus, using immunohistochemical and stereological techniques. Immunostaining for neuronal nuclear marker (NeuN) revealed substantial numbers of WMICs in each species-M. woermanni 124,496 WMICs, C. argynnis 138,458 WMICs, and the larger brained R. aegyptiacus having an estimated WMIC population of 360,503. To examine the range of inhibitory neurochemical types we used antibodies against parvalbumin, calbindin, calretinin, and neural nitric oxide synthase (nNOS). The calbindin and nNOS immunostained neurons were the most commonly observed, while those immunoreactive for calretinin and parvalbumin were sparse. The proportion of WMICs exhibiting inhibitory neurochemical profiles was ~26%, similar to that observed in previously studied primates. While for the most part the WMIC population in the megachiropterans studied was similar to that observed in other mammals, the one feature that differed was the high proportion of WMICs immunoreactive to calbindin, whereas in primates (macaque monkey, lar gibbon and human) the highest proportion of inhibitory WMICs contain calretinin. Interestingly, there appears to be an allometric scaling of WMIC numbers with brain mass. Further quantitative comparative work across more mammalian species will reveal the developmental and evolutionary trends associated with this infrequently studied neuronal population.

Intrinsic Ball Retrieving in Wolf Puppies Suggests Standing Ancestral Variation for Human-Directed Play Behavior.

SummaryDomestication dramatically alters phenotypes across animal species. Standing variation among ancestral populations often drives phenotypic change during domestication, but some changes are caused by novel mutations. In dogs (Canis familiaris) specifically, it has been suggested that the ability to interpret social-communicative behavior expressed by humans originated post-domestication and this behavior is thus not expected to occur in wolves (Canis lupus). Here we report the observation of three 8-week-old wolf puppies spontaneously responding to social-communicative behaviors from an unfamiliar person by retrieving a ball. This behavioral expression in wolves has significant implications for our understanding and expectations of the genetic foundations of dog behavior. Importantly, our observations indicate that behavioral responses to human social-communicative cues are not unique to dogs. This suggests that, although probably rare, standing variation in the expression of human-directed behavior in ancestral populations could have been an important target for early selective pressures exerted during dog domestication.

Megachiropteran bats profoundly unique from microchiropterans in climbing and walking locomotion: Evolutionary implications.

Understandably, most locomotor analyses of bats have focused on flight mechanics and behaviors. However, we investigated nonflight locomotion in an effort to glean deeper insights into the evolutionary history of bats. We used high-speed video (300 Hz) to film and compare walking and climbing mechanics and kinematics between several species of the suborders Megachiroptera (Pteropodidae) versus Microchiroptera (Vespertilionidae and Phyllostomatidae). We found fundamentally distinctive behaviors, functional abilities, and performance outcomes between groups, but nearly homogeneous outcomes within groups. Megachiropterans exhibited climbing techniques and skills not found in microchiropterans and which aligned with other fully arboreal mammals. Megachiropterans climbed readily when placed in a head-up posture on a vertical surface, showed significantly greater ability than microchiropterans to abduct and extend the reach of their limbs, and climbed at a greater pace by using a more aggressive ipsilateral gait, at times being supported by only a single contact point. In addition, megachiropterans showed little ability to employ basic walking mechanics when placed on the ground, also a pattern observed in some highly adapted arboreal mammals. Conversely, microchiropterans resisted climbing vertical surfaces in a head-up posture, showed significantly less extension of their limbs, and employed a less-aggressive, slower contralateral gait with three points of contact. When walking, microchiropterans used the same gait they did when climbing which is representative of basic tetrapod terrestrial mechanics. Curiously, megachiropterans cycled their limbs significantly faster when climbing than when attempting to walk, whereas microchiropterans cycled their limbs at significantly faster rates when walking than when climbing. We contend that nonflight locomotion mechanics give a deep evolutionary view into the ancestral es locomotor platform on which flight was built in each of these groups.

Eye Size and Set in Small-Bodied Fossil Primates: A Three-Dimensional Method.

We introduce a new method to geometrically reconstruct eye volume and placement in small-bodied primates based on the three-dimensional contour of the intraorbital surface. We validate it using seven species of living primates, with dry skulls and wet dissections, and test its application on seven species of Paleogene fossils of interest. The method performs well even when the orbit is damaged and incomplete, lacking the postorbital bar and represented only by the orbital floor. Eye volume is an important quantity for anatomic and metabolic reasons, which due to differences in eye set, or position within (or outside) the bony orbit, can be underestimated in living and fossil forms when calculated from aperture diameter. Our Ectopic Index quantifies how much the globe's volume protrudes anteriorly from the aperture. Lemur, Notharctus and Rooneyia resemble anthropoids, with deeply recessed eyes protruding 11%-13%. Galago and Tarsius are the other extreme, at 47%-56%. We argue that a laterally oriented aperture has little to do with line-of-sight in euprimates, as large ectopic eyes can position the cornea to enable a directly forward viewing axis, and soft tissue positions the eyes facing forward in megachiropteran bats, which have unenclosed, open eye sockets. The size and set of virtual eyes reconstructed from 3D cranial models confirm that eyes were large to hypertrophic in Hemiacodon, Necrolemur, Microchoerus, Pseudoloris and Shoshonius, but eye size in Rooneyia may have been underestimated by measuring the aperture, as in Aotus. Anat Rec, 299:1671-1689, 2016. © 2016 Wiley Periodicals, Inc.

ESTABLISHMENT OF REFERENCE INTERVALS FOR HEMATOLOGY AND BIOCHEMISTRY ANALYTES IN A CAPTIVE COLONY OF STRAW-COLORED FRUIT BATS (EIDOLON HELVUM).

Straw-colored fruit bats (Eidolon helvum) are an ecologically important species of megachiropteran bat that are common both in captivity and in the wild. This study attempts to determine reference intervals from a group of 45 captive individuals for a variety of hematologic and biochemistry parameters. Most of the values are similar to values previously seen in other pteropodid bat species. Differences included a lower than expected reference interval for the total white blood cell count, a wider reference interval for glucose, and a higher reference interval for 25-hydroxyvitamin D. Establishing reference intervals for hematologic and biochemistry analytes for bats that were maintained on the same diet and under the same husbandry parameters for several years will help in the future assessment of other bats maintained in a similar manner.

Keanekaragaman Jenis dan Pemanfaatan Sumberdaya oleh Kelelawar Sub Ordo Megachiroptera di Taman Wisata Alam Gunung Meja Manokwari, Papua Barat

Bats utilizing resources together will differ morphologically, ecologically, and behaviorally. This study aimed to measure species diversity and to investigate resource use by Megachiropteran bats. Data were analyzed using Principal Component Analysis (PCA), Canonical Correspondence Analysis (CCA), Correspondence Analysis (CA), euclidean distance, chi square, Anova, and niche overlap index. The result showed seven bat species were captured in three habitat types. Plant as food identified from pollen comprised 55 species from 29 families and 11 types of corolla. Dobsonia magna and Rousettus amplexicaudatus preferred mixed fruit plantation, whilst other bat species tended to choose primary forest. Dobsonia minor tended to have high niche overlap against Macroglossus minimus and Nyctemene aello. According to similarity of food resource niche, Dobsonia magna, Dobsonia minor, and Macroglossus minimus tended to closely associate, in contrast, Rousettus amplexicaudatus, Nyctemene albiventer, Nyctemene aello, and Syconicteris australis were grouped correspondingly. Niche overlap index of food resource among bat species were overall less than 50%. This indicated that there was no interspecies competition to food resource. Coronoid process height (CPH), maximum zygomatic breadth (MZB), and condyle to canine bite point (CC) were craniodental morphology variables which did not describe certain corolla types. Keywords: species diversity, resource use, niche overlap, Megachiropteran, Gunung Meja

Systemic toxoplasmosis in captive flying‐foxes

Systemic toxoplasmosis caused by Toxoplasma gondii was diagnosed in two juvenile, captive flying-foxes (Pteropus conspicillatus and P. scapulatus), which died following respiratory distress. One animal displayed clinical signs suggestive of neurological disease. This is the first report of this disease in megachiropteran bats and adds to the list of differential diagnoses for both systemic and neurological disease in these animals. The role of captivity in the exposure and development of the disease is discussed.

Megachiropteran bats (pteropus) utilize human referential stimuli to locate hidden food.

Spontaneous point-following behavior has been considered an indicator of advanced social cognition unique to humans. Recently, it has been suggested that a close evolutionary relationship with humans could result in similar social skills in domesticated species. An alternative view is that the mechanism is not genetic domestication alone but instead a combination of phylogenetic and ontogenetic variables. Here we test the necessity of phylogenetic domestication by investigating the point-following behavior of a captive population of nondomesticated megachiropteran bats (Pteropus pumilus, Pteropus rodricensis, Pteropus conspicillatus, Pteropus vampyrus). Three of five subjects were highly successful in following an unfamiliar human's point to a target location, providing the first empirical evidence of cross-species social referencing in bats. The three successful bats were all born in captivity and socialized to humans early in life, whereas unsuccessful bats were wild-born individuals. This study provides evidence that referential point following is not restricted to domesticated animals and indicates that early experience may be important. Megachiropteran bats may prove to be a useful model for studying social behaviors.

Chapter 6. Phylogenetic Relationships of Harpyionycterine Megabats (Chiroptera: Pteropodidae)

Abstract After almost 70 years of stability following publication of Andersen's (1912) monograph on the group, the systematics of megachiropteran bats (Chiroptera: Pteropodidae) was thrown into flux with the advent of molecular phylogenetics in the 1980s—a state where it has remained ever since. One particularly problematic group has been the Austromalayan Harpyionycterinae, currently thought to include Dobsonia and Harpyionycteris, and probably also Aproteles. In this contribution we revisit the systematics of harpyionycterines. We examine historical hypotheses of relationships including the suggestion by O. Thomas (1896) that the rousettine Boneia bidens may be related to Harpyionycteris, and report the results of a series of phylogenetic analyses based on new as well as previously published sequence data from the genes RAG1, RAG2, vWF, c-mos, cytb, 12S, tVal, 16S, and ND2. Despite a striking lack of morphological synapomorphies, results of our combined analyses indicate that Boneia groups with Aprotele...

The role of olfaction and vision in the foraging behaviour of an echolocating megachiropteran fruit bat, Rousettus leschenaulti (Pteropodidae)

Many mammals use multimodal sensory information to find their food in complex environments. We studied the roles of olfactory and visual cues in the foraging behaviour of Rousettus leschenaulti, a tongue-clicking megachiropteran bat. We conducted experiments by offering a whole fruit, mashed fruit without shape and an artificial fruit to R. leschenaulti in dim light as well as in total darkness. R. leschenaulti responded to whole guava fruit and mashed guava fruit even in total darkness, whereas, artificial fruit similar to real fruit in size, shape and structure was ignored even when illuminated. These results reveal that odour may act as the primary cue for R. leschenaulti in finding fruit.

Detection of specific antibody responses to vaccination in variable flying foxes (Pteropus hypomelanus)

Megachiropteran bats are biologically important both as endangered species and reservoirs for emerging human pathogens. Reliable detection of antibodies to specific pathogens in bats is thus epidemiologically critical. Eight variable flying foxes (Pteropus hypomelanus) were immunized with 2,4-dinitrophenylated bovine serum albumin (DNP-BSA). Each bat received monthly inoculations for 2 months. Affinity-purified IgG was used for production of polyclonal and monoclonal anti-variable flying fox IgG antibodies. ELISA and western blot analysis were used to monitor immune responses and for assessment of polyclonal and monoclonal antibody species cross-reactivity. Protein G, polyclonal antibodies, and monoclonal antibodies detected specific anti-DNP antibody responses in immunized variable flying foxes, with protein G being the most sensitive, followed by monoclonal antibodies and then polyclonal antibodies. While the polyclonal antibody was found to cross-react well against IgG of all bat species tested, some non-specific background was observed. The monoclonal antibody was found to cross-react well against IgG of six other species in the genus Pteropus and to cross-react less strongly against IgG from Eidolon helvum or Phyllostomus hastatus. Protein G distinguished best between vaccinated and unvaccinated bats, and these results validate the use of protein G for detection of bat IgG. Monoclonal antibodies developed in this study recognized immunoglobulins from other members of the genus Pteropus well, and may be useful in applications where specific detection of Pteropus IgG is needed.

The effect of familiarity on echolocation in the megachiropteran bat Rousettus aegyptiacus

Much is known about the way bats adjust their echolocation behaviour in response to environmental structure or to locate insect prey. By contrast, little is known about how echolocation calls are modulated in response to familiarity of the environment and objects within it. Here we show that the echolocating Megachiropteran bat Rousettus aegyptiacus produces echolocation signals at the same rate whether an obstacle is predictable or unpredictable in location, but that it has a reduced rate of echolocation signal production in a familiar environment with no obstacle present. This suggests that signal production is reduced in a familiar environment absent of 'clutter' but that probing the environment for maximum information is more important for this species than minimizing any cost of probing the environment in a cluttered space.

Element Homology and the Evolution of Dental Formulae in Megachiropteran Bats (Mammalia: Chiroptera: Pteropodidae)

Variation in dental formulae observed in megachiropteran bats poses element homology problems. Identity of individual teeth has been controversial, with authors differing in their assessment of individual tooth homology, particularly with respect to incisors and premolars, in several taxa. Also, newly described taxa exhibit dental formulae whose implications for tooth homology have been little discussed. We compared crown morphology, tooth replacement, and dental anomalies in representatives of all megachiropteran genera. Our observations confirm the generalized megachiropteran dental formula (34 teeth represented by I1, I2, C, P1, P3, P4, M1, M2, i1, i2, c, p1, p3, p4, m1, m2, and m3) and establishes the homology of each tooth in most megachiropteran taxa in which reduction in tooth number has taken place. Some of our conclusions confirm presumed homologies postulated by previous authors, but in other cases new homology assignments are proposed. Uncorroborated assignments are reduced to just two taxa, Harpyionycteris and Nyctimeninae, both of which remain problematic with respect to homologies of the incisor dentition. Mapping tooth presence/absence on previously published phylogenetic trees reveals modest levels of ambiguity and homoplasy in patterns of tooth reduction in Pteropodidae, and indicates that reversals involving the reappearance of an ancestrally lost tooth may have taken place. Our results are consistent with dental field theory, which explains both reversals and anomalies as a regulatory variation that does not affect element homology because the latter is supported by structural genes.

DEVELOPMENT OF INTEGUMENTARY STRUCTURES IN ROUSETTUS AMPLEXICAUDATUS (MAMMALIA: CHIROPTERA: PTEROPODIDAE) DURING LATE-EMBRYONIC AND FETAL STAGES

The pattern of development of integumentary structures and associated tissues in the megachiropteran bat Rousettus amplexicaudatus is described on the basis of 18 specimens ranging in crown–rump length (CRL) from 8.5 to 44.4 mm. The ontogenetic sample encompasses specimens that correspond to stages 16 through 22 of the phyllostomid Carollia perspicillata (late-embryonic) as well as fetal stages. Although the earlier stages of R. amplexicaudatus show little deviations in relative timing or anatomy from Carollia, later ones are increasingly different. Integumentary structures show different degrees of developmental penetrance. Derived features in embryonic stages are clearly reflected in adult structures such as a great enlargement of the handplate in relation to the footplate at the moment in which both are fully differentiated. We propose that patagium morphogenesis includes development of dactylopatagium by initial retention and posterior growth of interdigital tissue, coupled with digit elongation; and development of pro-, plagio-, and uropatagium in association with wing muscles unique to bats. Additionally, allometric trends in wingspan, total wing area, arm-wing area, and hand-wing area were estimated with respect to CRL. Changes in the terminology of some Carollia stages (16 and 18) are proposed to facilitate comparisons across bat species.

Olfactory discrimination ability of the short-nosed fruit bat Cynopterus sphinx

ABSTRACT We carried out a set of experiments on a megachiropteran bat Cynopterus sphinx to examine its olfactory discrimination ability to a variety of food odor substances. We used seven undiluted odorants such as isoamyl acetate, ethyl acetate, hexanol, benzaldehyde, limonene, pinene, and dimethyl disulfide for odor discrimination experiments. These volatile substances are present at various quantities in the natural food (fruits and nectar) of C. sphinx. Equal amount (200 μl) of seven odor substances kept individually but simultaneously in seven of eight specimen tubes which were equipped in a radially and horizontally arranged experimental set-up. In addition to the odorants, about 5 mm pieces of any one of the fruits such as guava, papaya and sapota were offered in cups as reward to the bats. The behavior of bats was observed visually and number of bat-visits to the odorants, and to the scentless control was continuously recorded in an event recorder. The mean number of approaches made by the bats di...