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Concept: Big brown bat

172

Bats are among the most gregarious and vocal mammals, with some species demonstrating a diverse repertoire of syllables under a variety of behavioral contexts. Despite extensive characterization of big brown bat (Eptesicus fuscus) biosonar signals, there have been no detailed studies of adult social vocalizations. We recorded and analyzed social vocalizations and associated behaviors of captive big brown bats under four behavioral contexts: low aggression, medium aggression, high aggression, and appeasement. Even limited to these contexts, big brown bats possess a rich repertoire of social vocalizations, with 18 distinct syllable types automatically classified using a spectrogram cross-correlation procedure. For each behavioral context, we describe vocalizations in terms of syllable acoustics, temporal emission patterns, and typical syllable sequences. Emotion-related acoustic cues are evident within the call structure by context-specific syllable types or variations in the temporal emission pattern. We designed a paradigm that could evoke aggressive vocalizations while monitoring heart rate as an objective measure of internal physiological state. Changes in the magnitude and duration of elevated heart rate scaled to the level of evoked aggression, confirming the behavioral state classifications assessed by vocalizations and behavioral displays. These results reveal a complex acoustic communication system among big brown bats in which acoustic cues and call structure signal the emotional state of a caller.

Concepts: Psychology, Sociology, Mammal, Acoustics, Bat, Big brown bat, Little brown bat, Eptesicus

64

Flight maneuvers require rapid sensory integration to generate adaptive motor output. Bats achieve remarkable agility with modified forelimbs that serve as airfoils while retaining capacity for object manipulation. Wing sensory inputs provide behaviorally relevant information to guide flight; however, components of wing sensory-motor circuits have not been analyzed. Here, we elucidate the organization of wing innervation in an insectivore, the big brown bat, Eptesicus fuscus. We demonstrate that wing sensory innervation differs from other vertebrate forelimbs, revealing a peripheral basis for the atypical topographic organization reported for bat somatosensory nuclei. Furthermore, the wing is innervated by an unusual complement of sensory neurons poised to report airflow and touch. Finally, we report that cortical neurons encode tactile and airflow inputs with sparse activity patterns. Together, our findings identify neural substrates of somatosensation in the bat wing and imply that evolutionary pressures giving rise to mammalian flight led to unusual sensorimotor projections.

Concepts: Nervous system, Sensory system, Sense, Somatosensory system, Bat, Proprioception, Big brown bat, Wing

24

The wing membrane of the big brown bat (Eptesicus fuscus) is covered by a sparse grid of microscopic hairs. We showed previously that various tactile receptors (e.g. lanceolate endings and Merkel cell neurite complexes) are associated with wing hair follicles. Furthermore, we found that depilation of these hairs decreased the maneuverability of bats in flight. In the present study, we investigated whether somatosensory signals arising from the hairs carry information about air flow parameters. Neural responses to calibrated air puffs on the wing were recorded from primary somatosensory cortex of Eptesicus fuscus. Single units showed sparse, phasic, and consistently timed spikes that were insensitive to air puff duration and magnitude. The neurons discriminated airflow from different directions and a majority responded with highest firing rates to reverse airflow from the trailing toward the leading edge of the dorsal wing. Reverse airflow, caused by vortices, occurs commonly in slowly flying bats. Hence, the present findings suggest that cortical neurons are specialized to monitor reverse airflow, indicating laminar airflow disruption (vorticity) that potentially destabilizes flight and leads to stall.

Concepts: Time, Cerebral cortex, Somatosensory system, Bat, Big brown bat, Flight, Wing, Flying and gliding animals

10

The bat-moth arms race has existed for over 60 million y, with moths evolving ultrasonically sensitive ears and ultrasound-producing organs to combat bat predation. The evolution of these defenses has never been thoroughly examined because of limitations in simultaneously conducting behavioral and phylogenetic analyses across an entire group. Hawkmoths include >1,500 species worldwide, some of which produce ultrasound using genital stridulatory structures. However, the function and evolution of this behavior remain largely unknown. We built a comprehensive behavioral dataset of hawkmoth hearing and ultrasonic reply to sonar attack using high-throughput field assays. Nearly half of the species tested (57 of 124 species) produced ultrasound to tactile stimulation or playback of bat echolocation attack. To test the function of ultrasound, we pitted big brown bats (Eptesicus fuscus) against hawkmoths over multiple nights and show that hawkmoths jam bat sonar. Ultrasound production was immediately and consistently effective at thwarting attack and bats regularly performed catching behavior without capturing moths. We also constructed a fossil-calibrated, multigene phylogeny to study the evolutionary history and divergence times of these antibat strategies across the entire family. We show that ultrasound production arose in multiple groups, starting in the late Oligocene (∼26 Ma) after the emergence of insectivorous bats. Sonar jamming and bat-detecting ears arose twice, independently, in the Miocene (18-14 Ma) either from earless hawkmoths that produced ultrasound in response to physical contact only, or from species that did not respond to touch or bat echolocation attack.

Concepts: Evolution, Biology, Insect, Ultrasound, Animal echolocation, Bat, Big brown bat, Microbat

8

Adaptations to divert the attacks of visually guided predators have evolved repeatedly in animals. Using high-speed infrared videography, we show that luna moths (Actias luna) generate an acoustic diversion with spinning hindwing tails to deflect echolocating bat attacks away from their body and toward these nonessential appendages. We pit luna moths against big brown bats (Eptesicus fuscus) and demonstrate a survival advantage of ∼47% for moths with tails versus those that had their tails removed. The benefit of hindwing tails is equivalent to the advantage conferred to moths by bat-detecting ears. Moth tails lured bat attacks to these wing regions during 55% of interactions between bats and intact luna moths. We analyzed flight kinematics of moths with and without hindwing tails and suggest that tails have a minimal role in flight performance. Using a robust phylogeny, we find that long spatulate tails have independently evolved four times in saturniid moths, further supporting the selective advantage of this anti-bat strategy. Diversionary tactics are perhaps more common than appreciated in predator-prey interactions. Our finding suggests that focusing on the sensory ecologies of key predators will reveal such countermeasures in prey.

Concepts: Evolution, Insect, Predation, Ecology, Bat, Big brown bat, Moth, Actias luna

6

Invasive insect pests cost the agricultural industry billions of dollars annually in crop losses. Timely detection of pests is critical for management efficiency. Innovative pest detection strategies, such as environmental DNA (eDNA) techniques, combined with efficient predators, maximize sampling resolution across space and time and may improve surveillance. We tested the hypothesis that temperate insectivorous bats can be important sentinels of agricultural insect pest surveillance. Specifically, we used a new high-sensitivity molecular assay for invasive brown marmorated stink bugs (Halyomorpha halys) to examine the extent to which big brown bats (Eptesicus fuscus) detect agricultural pests in the landscape. We documented consistent seasonal predation of stink bugs by big brown bats. Importantly, bats detected brown marmorated stink bugs 3-4 weeks earlier than the current standard monitoring tool, blacklight traps, across all sites. We highlight here the previously unrecognized potential ecosystem service of bats as agents of pest surveillance (or chirosurveillance). Additional studies examining interactions between other bat and insect pest species, coupled with comparisons of detectability among various conventional monitoring methods, are needed to verify the patterns extracted from this study. Ultimately, robust economic analyses will be needed to assess the cost-effectiveness of chirosurveillance as a standard strategy for integrated pest management.

Concepts: Biodiversity, Agriculture, Insect, Animal echolocation, Bat, Big brown bat, Pest control, Insectivore

5

This study investigated auditory stimulus selectivity in the midbrain superior colliculus (SC) of the echolocating bat, an animal that relies on hearing to guide its orienting behaviors. Multichannel, single-unit recordings were taken across laminae of the midbrain SC of the awake, passively listening big brown bat, Eptesicus fuscus. Species-specific frequency-modulated (FM) echolocation sound sequences with dynamic spectrotemporal features served as acoustic stimuli along with artificial sound sequences matched in bandwidth, amplitude, and duration but differing in spectrotemporal structure. Neurons in dorsal sensory regions of the bat SC responded selectively to elements within the FM sound sequences, whereas neurons in ventral sensorimotor regions showed broad response profiles to natural and artificial stimuli. Moreover, a generalized linear model (GLM) constructed on responses in the dorsal SC to artificial linear FM stimuli failed to predict responses to natural sounds and vice versa, but the GLM produced accurate response predictions in ventral SC neurons. This result suggests that auditory selectivity in the dorsal extent of the bat SC arises through nonlinear mechanisms, which extract species-specific sensory information. Importantly, auditory selectivity appeared only in responses to stimuli containing the natural statistics of acoustic signals used by the bat for spatial orientation-sonar vocalizations-offering support for the hypothesis that sensory selectivity enables rapid species-specific orienting behaviors. The results of this study are the first, to our knowledge, to show auditory spectrotemporal selectivity to natural stimuli in SC neurons and serve to inform a more general understanding of mechanisms guiding sensory selectivity for natural, goal-directed orienting behaviors.

Concepts: Scientific method, Auditory system, Ultrasound, Animal echolocation, Generalized linear model, Sound, Big brown bat, Eptesicus

5

Animals foraging in the dark are engaged simultaneously in prey pursuit, collision avoidance, and interactions with conspecifics, making efficient nonvisual communication essential. A variety of birds and mammals emit food-associated calls that inform, attract, or repel conspecifics (e.g., [1]). Big brown bats (Eptesicus fuscus) are insectivorous aerial hawkers that may forage near conspecifics and are known to emit social calls (e.g., [2-5]). Calls recorded in a foraging setting might attract (e.g., [6]) or repel [7] conspecifics and could denote territoriality or food claiming. Here, we provide evidence that the “frequency-modulated bout” (FMB), a social call emitted only by male bats (exclusively in a foraging context) [5], is used to claim food and is individually distinct. Bats were studied individually and in pairs in a flight room equipped with synchronized high-speed stereo video and audio recording equipment while sex and experience with a foraging task were experimentally manipulated. Male bats emitting the FMB showed greater success in capturing prey. Following FMB emission, interbat distance, diverging flight, and the other bat’s distance to the prey each increased. These findings highlight the importance and utility of vocal communication for a nocturnal animal mediating interactions with conspecifics in a fast-paced foraging setting.

Concepts: Insect, Mammal, Communication, Bat, Ethology, Big brown bat, Flying and gliding animals, Bats

3

In many vertebrates, exposure to intense sounds under certain stimulus conditions can induce temporary threshold shifts that reduce hearing sensitivity. Susceptibility to these hearing losses may reflect the relatively quiet environments in which most of these species have evolved. Echolocating big brown bats (Eptesicus fuscus) live in extremely intense acoustic environments in which they navigate and forage successfully, both alone and in company with other bats. We hypothesized that bats may have evolved a mechanism to minimize noise-induced hearing losses that otherwise could impair natural echolocation behaviors. The hearing sensitivity of seven big brown bats was measured in active echolocation and passive hearing tasks, before and after exposure to broadband noise spanning their audiometric range (10-100 kHz, 116 dB SPL re. 20 µPa rms, 1 h duration; sound exposure level 152 dB). Detection thresholds measured 20 min, 2 h or 24 h after exposure did not vary significantly from pre-exposure thresholds or from thresholds in control (sham exposure) conditions. These results suggest that big brown bats may be less susceptible to temporary threshold shifts than are other terrestrial mammals after exposure to similarly intense broadband sounds. These experiments provide fertile ground for future research on possible mechanisms employed by echolocating bats to minimize hearing losses while orienting effectively in noisy biological soundscapes.

Concepts: Mammal, Acoustics, Ultrasound, Animal echolocation, Sound, Bat, Hearing, Big brown bat

2

Rabies is an ancient neglected tropical disease that causes tens of thousands of human deaths and millions of cattle deaths annually. In order to develop a new vaccine for potential use in bats, a reservoir of rabies infection for humans and animals alike, an in silico antigen designer tool was used to create a mosaic glycoprotein (MoG) gene using available sequences from the rabies Phylogroup I glycoprotein. This sequence, which represents strains more likely to occur in bats, was cloned into raccoonpox virus (RCN) and the efficacy of this novel RCN-MoG vaccine was compared to RCN-G that expresses the glycoprotein gene from CVS-11 rabies or luciferase (RCN-luc, negative control) in mice and big brown bats (Eptesicus fuscus). Mice vaccinated and boosted intradermally with 1 x 107 plaque forming units (PFU) of each RCN-rabies vaccine construct developed neutralizing antibodies and survived at significantly higher rates than controls. No significant difference in antibody titers or survival was noted between rabies-vaccinated groups. Bats were vaccinated either oronasally (RCN-G, RCN-MoG) with 5x107 PFU or by topical application in glycerin jelly (RCN-MoG, dose 2x108 PFU), boosted (same dose and route) at 46 days post vaccination (dpv), and then challenged with wild-type big brown variant RABV at 65 dpv. Prior to challenge, 90% of RCN-G and 75% of RCN-MoG oronasally vaccinated bats had detectable levels of serum rabies neutralizing antibodies. Bats from the RCN-luc and topically vaccinated RCN-MoG groups did not have measurable antibody responses. The RCN-rabies constructs were highly protective and not significantly different from each other. RCN-MoG provided 100% protection (n = 9) when delivered oronasally and 83% protection (n = 6) when delivered topically; protection provided by the RCN-G construct was 70% (n = 10). All rabies-vaccinated bats survived at a significantly (P ≤ 0.02) higher rate than control bats (12%; n = 8). We have demonstrated the efficacy of a novel, in silico designed rabies MoG antigen that conferred protection from rabies challenge in mice and big brown bats in laboratory studies. With further development, topical or oronasal administration of the RCN-MoG vaccine could potentially mitigate rabies in wild bat populations, reducing spillover of this deadly disease into humans, domestic mammals, and other wildlife.

Concepts: Immune system, Antibody, Vaccine, Vaccination, Topical, Smallpox, Rabies, Big brown bat