Multi-year soundscape recordings and automated call detection reveals varied impact of moonlight on calling activity of neotropical forest katydids.

Night-time light can have profound ecological effects, even when the source is natural moonlight. The impacts of light can, however, vary substantially by taxon, habitat and geographical region. We used a custom machine learning model built with the Python package Koogu to investigate the in situ effects of moonlight on the calling activity of neotropical forest katydids over multiple years. We prioritised species with calls that were commonly detected in human annotated data, enabling us to evaluate model performance. We focused on eight species of katydids that the model identified with high precision (generally greater than 0.90) and moderate-to-high recall (minimum 0.35), ensuring that detections were generally correct and that many calls were detected. These results suggest that moonlight has modest effects on the amount of calling, with the magnitude and direction of effect varying by species: half of the species showed positive effects of light and half showed negative. These findings emphasize the importance of understanding natural history for anticipating how biological communities respond to moonlight. The methods applied in this project highlight the emerging opportunities for evaluating large quantities of data with machine learning models to address ecological questions over space and time. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

Ear pinnae in a neotropical katydid (Orthoptera: Tettigoniidae) function as ultrasound guides for bat detection.

Early predator detection is a key component of the predator-prey arms race and has driven the evolution of multiple animal hearing systems. Katydids (Insecta) have sophisticated ears, each consisting of paired tympana on each foreleg that receive sound both externally, through the air, and internally via a narrowing ear canal running through the leg from an acoustic spiracle on the thorax. These ears are pressure-time difference receivers capable of sensitive and accurate directional hearing across a wide frequency range. Many katydid species have cuticular pinnae which form cavities around the outer tympanal surfaces, but their function is unknown. We investigated pinnal function in the katydid Copiphora gorgonensis by combining experimental biophysics and numerical modelling using 3D ear geometries. We found that the pinnae in C. gorgonensis do not assist in directional hearing for conspecific call frequencies, but instead act as ultrasound detectors. Pinnae induced large sound pressure gains (20-30 dB) that enhanced sound detection at high ultrasonic frequencies (>60 kHz), matching the echolocation range of co-occurring insectivorous gleaning bats. These findings were supported by behavioural and neural audiograms and pinnal cavity resonances from live specimens, and comparisons with the pinnal mechanics of sympatric katydid species, which together suggest that katydid pinnae primarily evolved for the enhanced detection of predatory bats.

Hearing sensitivity: An underlying mechanism for niche differentiation in gleaning bats.

Tropical ecosystems are known for high species diversity. Adaptations permitting niche differentiation enable species to coexist. Historically, research focused primarily on morphological and behavioral adaptations for foraging, roosting, and other basic ecological factors. Another important factor, however, is differences in sensory capabilities. So far, studies mainly have focused on the output of behavioral strategies of predators and their prey preference. Understanding the coexistence of different foraging strategies, however, requires understanding underlying cognitive and neural mechanisms. In this study, we investigate hearing in bats and how it shapes bat species coexistence. We present the hearing thresholds and echolocation calls of 12 different gleaning bats from the ecologically diverse Phyllostomid family. We measured their auditory brainstem responses to assess their hearing sensitivity. The audiograms of these species had similar overall shapes but differed substantially for frequencies below 9 kHz and in the frequency range of their echolocation calls. Our results suggest that differences among bats in hearing abilities contribute to the diversity in foraging strategies of gleaning bats. We argue that differences in auditory sensitivity could be important mechanisms shaping diversity in sensory niches and coexistence of species.

Predation risks of signalling and searching: bats prefer moving katydids.

Males signalling their attractiveness to females are at risk from predators that exploit mating signals to detect and locate prey. Signalling, however, is not the only risky activity in sexual interactions: mate searching can incur risk as well. Male Neotropical pseudophylline katydids produce both acoustic and vibrational signals (tremulations). Females reply to male signals with tremulations of their own, and both sexes walk to find one another. We asked if movement increases predation risk, and whether tremulation or walking was more attractive to predators. We offered the Neotropical gleaning bat Micronycteris microtis a series of two-choice tests, presenting the bats with katydid models that were motionless or moved in a way to mimic either tremulating or walking. We found that prey movements do put prey at risk. Although M. microtis can detect motionless prey on leaves, they preferred moving prey. Our study shows that movement can put searching or signalling prey in danger, potentially explaining why silent female katydids are frequently consumed by gleaning bats.

Bats Actively Use Leaves as Specular Reflectors to Detect Acoustically Camouflaged Prey.

Filtering relevant signals from noisy sensory input is a crucial challenge for animals [1, 2]. Many bats are acoustic specialists relying on sound to find prey. They discern salient acoustic signals from irrelevant background masking noise. It has long been considered a sensory impossibility for bats to use solely echolocation for the detection of silent and motionless prey resting directly on foliage due to the masking effects of background echoes [3, 4]. Some bats, however, do successfully perform this seemingly impossible task [5], raising the question-what underlying acoustic and behavioral mechanisms do bats use to solve this conundrum? To address this question, we used biomimetic sonar to record high-resolution measurements of echoes from insects resting on leaves. Based on our echo recordings, we predicted optimal approach angles from which masking echoes can best be avoided. In behavioral experiments, we put these predictions to test. We recorded the prey approach behavior of wild bats in a flight cage equipped with an ultrasonic microphone synchronized with two high-speed cameras for 3D flightpath reconstructions. Bats approached prey from our predicted optimal oblique angles, using the leaf as a specular reflector to uncover previously acoustically hidden prey. Our findings disclose key behavioral and acoustic mechanisms enabling the detection of prey echoes that background clutter would otherwise mask. This work adds to the fundamental understanding of how bat echolocation strategies can override acoustic camouflage by silent, motionless prey, thus providing new insights into the evolutionary arms race between predators and their prey.

Noise as an informational cue for decision-making: the sound of rain delays bat emergence.

Background noise can have strong negative consequences for animals, reducing individual fitness by masking communication signals, impeding prey detection and increasing predation risk. While the negative impacts of noise across taxa have been well documented, the use of noise as an informational cue, providing animals with reliable information on environmental conditions, has been less well studied. In the tropical rainforest, downpours can be intense and frequent. Strong rainfall may impede efficient orientation and foraging for bats that need echolocation to both navigate and detect prey, and can result in higher flight costs due to increased metabolic rates. Using playback experiments at natural roosts, we tested whether two bat species, differing in their hunting strategies and foraging habitats, use rain noise as a cue to delay emergence from their roosts. We found that both species significantly delayed their emergence time during rain noise playbacks versus silence and ambient noise controls. We conclude that bats can use background noise, here the acoustic component of rainfall, as a reliable informational cue to make informed decisions, in this case about whether to initiate foraging trips or remain in the shelter of their roosts. Our findings suggest that environmental background noise can sometimes be beneficial to animals, in particular in situations where other sensory cues may be absent.

Low-cost synchronization of high-speed audio and video recordings in bio-acoustic experiments.

In this paper, we present a method for synchronizing high-speed audio and video recordings of bio-acoustic experiments. By embedding a random signal into the recorded video and audio data, robust synchronization of a diverse set of sensor streams can be performed without the need to keep detailed records. The synchronization can be performed using recording devices without dedicated synchronization inputs. We demonstrate the efficacy of the approach in two sets of experiments: behavioral experiments on different species of echolocating bats and the recordings of field crickets. We present the general operating principle of the synchronization method, discuss its synchronization strength and provide insights into how to construct such a device using off-the-shelf components.

Environmental conditions limit attractiveness of a complex sexual signal in the túngara frog.

Animals choosing particular display sites often balance sexual and natural selection pressures. Here we assess how physical properties of display sites can alter this balance by influencing signal production and attractiveness of the túngara frog (Physalaemus pustulosus). Males that call from very shallow water bodies (few mm depth) benefit from reduced predation risk, but by manipulating water levels, we show that this comes at a cost of reduced attractiveness to females. Our data show that calling from shallower water reduces a male's ability to float, limits the inflation of his vocal sac, and consequently reduces signal conspicuousness in terms of amplitude and complexity. Our results demonstrate that display site properties can set limits on signal production and attractiveness and may hence influence signal evolution. Signallers may shift between sites or engineer their display location, which can play a crucial role in signal divergence and speciation, particularly in a rapidly changing world.

The noseleaf of Rhinolophus formosae focuses the Frequency Modulated (FM) component of the calls.

Bats of the family Rhinolophidae emit their echolocation calls through their nostrils and feature elaborate noseleaves shaping the directionality of the emissions. The calls of these bats consist of a long constant-frequency component preceded and/or followed by short frequency-modulated sweeps. While Rhinolophidae are known for their physiological specializations for processing the constant frequency part of the calls, previous evidence suggests that the noseleaves of these animals are tuned to the frequencies in the frequency modulated components of the calls. In this paper, we seek further support for this hypothesis by simulating the emission beam pattern of the bat Rhinolophus formosae. Filling the furrows of lancet and removing the basal lappets (i.e., two flaps on the noseleaf) we find that these conspicuous features of the noseleaf focus the emitted energy mostly for frequencies in the frequency-modulated components. Based on the assumption that this component of the call is used by the bats for ranging, we develop a qualitative model to assess the increase in performance due to the furrows and/or the lappets. The model confirms that both structures decrease the ambiguity in selecting relevant targets for ranging. The lappets and the furrows shape the emission beam for different spatial regions and frequency ranges. Therefore, we conclude that the presented evidence is in line with the hypothesis that different parts of the noseleaves of Rhinolophidae are tuned to different frequency ranges with at least some of the most conspicuous ones being tuned to the frequency modulated components of the calls-thus yielding strong evidence for the sensory importance of the component.

Perception of silent and motionless prey on vegetation by echolocation in the gleaning bat Micronycteris microtis.

Gleaning insectivorous bats that forage by using echolocation within dense forest vegetation face the sensorial challenge of acoustic masking effects. Active perception of silent and motionless prey in acoustically cluttered environments by echolocation alone has thus been regarded impossible. The gleaning insectivorous bat Micronycteris microtis however, forages in dense understory vegetation and preys on insects, including dragonflies, which rest silent and motionless on vegetation. From behavioural experiments, we show that M. microtis uses echolocation as the sole sensorial modality for successful prey perception within a complex acoustic environment. All individuals performed a stereotypical three-dimensional hovering flight in front of prey items, while continuously emitting short, multi-harmonic, broadband echolocation calls. We observed a high precision in target localization which suggests that M. microtis perceives a detailed acoustic image of the prey based on shape, surface structure and material. Our experiments provide, to our knowledge, the first evidence that a gleaning bat uses echolocation alone for successful detection, classification and precise localization of silent and motionless prey in acoustic clutter. Overall, we conclude that the three-dimensional hovering flight of M. microtis in combination with a frequent emission of short, high-frequency echolocation calls is the key for active prey perception in acoustically highly cluttered environments.

All you can eat: high performance capacity and plasticity in the common big-eared bat, Micronycteris microtis (Chiroptera: Phyllostomidae).

Ecological specialization and resource partitioning are expected to be particularly high in the species-rich communities of tropical vertebrates, yet many species have broader ecological niches than expected. In Neotropical ecosystems, Neotropical leaf-nosed bats (Phyllostomidae) are one of the most ecologically and functionally diverse vertebrate clades. Resource partitioning in phyllostomids might be achieved through differences in the ability to find and process food. We selected Micronycteris microtis, a very small (5-7 g) animalivorous phyllostomid, to explore whether broad resource use is associated with specific morphological, behavioral and performance traits within the phyllostomid radiation. We documented processing of natural prey and measured bite force in free-ranging M. microtis and other sympatric phyllostomids. We found that M. microtis had a remarkably broad diet for prey size and hardness. For the first time, we also report the consumption of vertebrates (lizards), which makes M. microtis the smallest carnivorous bat reported to date. Compared to other phyllostomids, M. microtis had the highest bite force for its size and cranial shape and high performance plasticity. Bite force and cranial shape appear to have evolved rapidly in the M. microtis lineage. High performance capacity and high efficiency in finding motionless prey might be key traits that allow M. microtis, and perhaps other species, to successfully co-exist with other gleaning bats.

What noseleaves do for FM bats depends on their degree of sensorial specialization.

BACKGROUND: Many bats vocalizing through their nose carry a prominent noseleaf that is involved in shaping the emission beam of these animals. To our knowledge, the exact role of these appendages has not been thoroughly investigated as for no single species both the hearing and the emission spatial sensitivities have been obtained. In this paper, we set out to evaluate the complete spatial sensitivity of two species of New World leaf-nosed bats: Micronycteris microtis and Phyllostomus discolor. From an ecological point of view, these species are interesting as they belong to the same family (Phyllostomidae) and their noseleaves are morphologically similar. They differ vastly in the niche they occupy. Comparing these species allows us to relate differences in function of the noseleaf to the ecological background of bat species. METHODOLOGY/PRINCIPAL FINDINGS: We simulate the spatial sensitivity of both the hearing and the emission subsystems of two species, M. microtis and P. discolor. This technique allows us to evaluate the respective roles played by the noseleaf in the echolocation system of these species. We find that the noseleaf of M. microtis focuses the radiated energy better and yields better control over the emission beam. CONCLUSIONS: From the evidence presented we conclude that the noseleaves serve quantitatively different functions for different bats. The main function of the noseleaf is to serve as an energy focusing mechanism that increases the difference between the reflected energy from objects in the focal area and objects in the periphery. However, despite the gross morphological similarities between the noseleaves of the two Phyllostomid species they focus the energy to a different extent, a capability that can be linked to the different ecological niches occupied by the two species.