Relation of connectome topology to brain volume across 103 mammalian species.

The brain connectome is an embedded network of anatomically interconnected brain regions, and the study of its topological organization in mammals has become of paramount importance due to its role in scaffolding brain function and behavior. Unlike many other observable networks, brain connections incur material and energetic cost, and their length and density are volumetrically constrained by the skull. Thus, an open question is how differences in brain volume impact connectome topology. We address this issue using the MaMI database, a diverse set of mammalian connectomes reconstructed from 201 animals, covering 103 species and 12 taxonomy orders, whose brain size varies over more than 4 orders of magnitude. Our analyses focus on relationships between volume and modular organization. After having identified modules through a multiresolution approach, we observed how connectivity features relate to the modular structure and how these relations vary across brain volume. We found that as the brain volume increases, modules become more spatially compact and dense, comprising more costly connections. Furthermore, we investigated how spatial embedding shapes network communication, finding that as brain volume increases, nodes' distance progressively impacts communication efficiency. We identified modes of variation in network communication policies, as smaller and bigger brains show higher efficiency in routing- and diffusion-based signaling, respectively. Finally, bridging network modularity and communication, we found that in larger brains, modular structure imposes stronger constraints on network signaling. Altogether, our results show that brain volume is systematically related to mammalian connectome topology and that spatial embedding imposes tighter restrictions on larger brains.

Species and habitat specific changes in bird activity in an urban environment during Covid 19 lockdown.

Covid-19 lockdowns provided ecologists with a rare opportunity to examine how animals behave when humans are absent. Indeed many studies reported various effects of lockdowns on animal activity, especially in urban areas and other human-dominated habitats. We explored how Covid-19 lockdowns in Israel have influenced bird activity in an urban environment by using continuous acoustic recordings to monitor three common bird species that differ in their level of adaptation to the urban ecosystem: (1) the hooded crow, an urban exploiter, which depends heavily on anthropogenic resources; (2) the rose-ringed parakeet, an invasive alien species that has adapted to exploit human resources; and (3) the graceful prinia, an urban adapter, which is relatively shy of humans and can be found in urban habitats with shrubs and prairies. Acoustic recordings provided continuous monitoring of bird activity without an effect of the observer on the animal. We performed dense sampling of a 1.3 square km area in northern Tel-Aviv by placing 17 recorders for more than a month in different micro-habitats within this region including roads, residential areas and urban parks. We monitored both lockdown and no-lockdown periods. We portray a complex dynamic system where the activity of specific bird species depended on many environmental parameters and decreases or increases in a habitat-dependent manner during lockdown. Specifically, urban exploiter species decreased their activity in most urban habitats during lockdown, while human adapter species increased their activity during lockdown especially in parks where humans were absent. Our results also demonstrate the value of different habitats within urban environments for animal activity, specifically highlighting the importance of urban parks. These species- and habitat-specific changes in activity might explain the contradicting results reported by others who have not performed a habitat specific analysis.

Lockdowns due to the COVID-19 pandemic reduced human activity in early 2020, providing a rare opportunity to examine how wildlife behaves when humans are absent. While several studies reported increased abundance of animals in urban habitats, others cast doubt on these reports. Variation in study conclusions could be due to different species showing different levels of adaptation to human activity. Additionally, studies that rely on visually observing animals can impact their behavior and those based on public reporting may also have been influenced by changes in human activity. Therefore, it remained unclear whether COVID-19 lockdowns impacted wildlife and how this might differ among species. To quantify wildlife presence and activity during lockdown, Sun et al. placed recording devices in different urban environments, including roads, residential areas, and urban parks across Tel Aviv in Israel during early 2020. This allowed continuous monitoring of bird vocalizations during lockdown and non-lockdown periods and ensured the birds were not disturbed by human observers. Three common bird species, which each show different levels of adaptation to urban ecosystems, were monitored. The hooded crow, which depends heavily on human resources, and the rose-ringed parakeet, an invasive alien species which has adapted to exploit human resources, decreased their activity in most urban habitats during lockdowns. On the other hand, the graceful prinia, which has adapted to thrive in urban green spaces but is relatively shy of humans, showed increased activity, especially in parks where humans were absent. The findings of Sun et al. reveal that birds show species- and habitat-specific changes to their behavior as a result of decreased human activity. This might explain why previous studies ­ which did not perform habitat-specific analyses ­ gave conflicting reports of the impact of COVID-19 lockdowns on wildlife activity. The results also demonstrate the value of different habitats within urban environments for animal activity, specifically identifying the importance of urban parks. By highlighting the impact of human activity on urban wildlife, the findings provide a scientific basis for future conservation efforts.

Fruit bats adjust their decision-making process according to environmental dynamics.

One of the main functions of behavioral plasticity lies in the ability to contend with dynamic environments. Indeed, while numerous studies have shown that animals adapt their behavior to the environment, how they adapt their latent learning and decision strategies to changes in the environment is less understood. Here, we used a controlled experiment to examine the bats' ability to adjust their decision strategy according to the environmental dynamics. Twenty-five Egyptian fruit bats were placed individually in either a stable or a volatile environment for four consecutive nights. In the stable environment, two feeders offered food, each with a different reward probability (0.2 vs. 0.8) that remained fixed over two nights and were then switched, while in the volatile environment, the positions of the more and the less rewarding feeders were changed every hour. We then fit two alternative commonly used models namely, reinforcement learning and win-stay-lose-shift strategies to the bats' behavior. We found that while the bats adapted their decision-making strategy to the environmental dynamics, they seemed to be limited in their responses based on natural priors. Namely, when the environment had changed slowly, at a rate that is natural for these bats, they seemed to rely on reinforcement learning and their performance was nearly optimal, but when the experimental environment changed much faster than in the natural environment, the bats stopped learning and switched to a random decision-making strategy. Together, these findings exemplify both the bats' decision-making plasticity as well as its natural limitations.

What determines the information update rate in echolocating bats.

The rate of sensory update is one of the most important parameters of any sensory system. The acquisition rate of most sensory systems is fixed and has been optimized by evolution to the needs of the animal. Echolocating bats have the ability to adjust their sensory update rate which is determined by the intervals between emissions - the inter-pulse intervals (IPI). The IPI is routinely adjusted, but the exact factors driving its regulation are unknown. We use on-board audio recordings to determine how four species of echolocating bats with different foraging strategies regulate their sensory update rate during commute flights. We reveal strong correlations between the IPI and various echolocation and movement parameters. Specifically, the update rate increases when the signals' peak-energy frequency and intensity increases while the update rate decreases when flight speed and altitude increases. We suggest that bats control their information update rate according to the behavioral mode they are engaged in, while always maintaining sensory continuity. Specifically, we suggest that bats apply two modes of attention during commute flights. Our data moreover suggests that bats emit echolocation signals at accurate intervals without the need for external feedback.

Comparison of antiviral responses in two bat species reveals conserved and divergent innate immune pathways.

Bats host a range of disease-causing viruses without displaying clinical symptoms. The mechanisms behind this are a continuous source of interest. Here, we studied the antiviral response in the Egyptian fruit bat and Kuhl's pipistrelle, representing two subordinal clades. We profiled the antiviral response in fibroblasts using RNA sequencing and compared bat with primate and rodent responses. Both bats upregulate similar genes; however, a subset of these genes is transcriptionally divergent between them. These divergent genes also evolve rapidly in sequence, have specific promoter architectures, and are associated with programs underlying tolerance and resistance. Finally, we characterized antiviral genes that expanded in bats, with duplicates diverging in sequence and expression. Our study reveals a largely conserved antiviral program across bats and points to a set of genes that rapidly evolve through multiple mechanisms. These can contribute to bat adaptation to viral infection and provide directions to understanding the mechanisms behind it.

AI and the Doctor Dolittle challenge.

Talking to animals is a fundamental human desire. The emergence of powerful AI algorithms, and specifically Large Language Models, has driven many to suggest that we are on the verge of fulfilling this wish. A few large scientific consortia have been formed around this topic and several commercial entities even offer such services. We frame the task of communicating with animals as 'The Doctor Dolittle challenge' and identify three main obstacles on the route to doing so. First, although generative AI models can create novel animal communication samples, it is very difficult to determine their context, and we will forever be biased by our human umwelt when doing so. Second, using AI to extract context in an unsupervised manner must be validated through controlled experiments aiming to measure the animals' response. This is difficult, and moreover, AI algorithms tend to cling on to any available information and are thus prone to finding spurious correlations. And third, animal communication focuses on a restricted set of contexts, such as alarm and courtship, highly limiting our ability to communicate regarding other contexts. Nevertheless, using the tremendous power of novel AI methods to decipher and mimic animal communication is both fascinating and important. We thus define the criteria for passing the Doctor Dolittle challenge and call upon scientists to take on the mission.

Experiencing without knowing? Empirical evidence for phenomenal consciousness without access.

Can one have a phenomenal experience to which one does not have access? That is, can you experience something without knowing? The dissociation between phenomenal (P) and access (A) consciousness is widely debated. A major challenge to the supporters of this dissociation is the apparent inability to experimentally demonstrate that P-without-A consciousness exists; once participants report having a P-experience, they already have access to it. Thus, all previous empirical support for this dissociation is indirect. Here, using a novel paradigm, we create a situation where participants (Experiment 1, N = 40) lack online access to the stimulus yet are nevertheless able to retrospectively form judgements on its phenomenal, qualitative aspects. We further show that their performance cannot be fully explained by unconscious processing or by a response to stimulus offset (Experiment 2, N = 40). This suggests that P and A consciousness are not only conceptually distinct, but might also be teased apart empirically. STATEMENT OF RELEVANCE: A critical question in the scientific quest towards solving the problem of consciousness focuses on the ability to isolate conscious experiences at their purity, without any accompanying cognitive processes. This challenge has been augmented by a highly influential - yet controversial - dissociation suggested by the philosopher Ned Block between Phenomenal consciousness, or the "what it is like" to have an experience, and Access consciousness, indexing the ability to report that one has that experience. Critically, these two types of consciousness most typically go together, making it highly difficult - if not impossible - to isolate Phenomenal consciousness. Our work shows that the dissociation between phenomenal and access consciousness is not merely conceptual, but can also be empirically demonstrated. It further opens the gate to future studies pinpointing the neural correlates of the two types of consciousness.

Bat vocal sequences enhance contextual information independently of syllable order.

Many animals, humans included, rely on acoustic vocalizations for communication. The complexity of non-human vocal communication has been under debate one of the main open questions being: What could be the function of multi-syllabic vocal sequences? We address these questions by analyzing fruit-bat vocal communication. We use neural networks to encode the vocalizations, and statistical models to examine the information conveyed by sequences of vocalizations. We show that fruit-bat vocal sequences potentially convey more contextual information than individual syllables, but that the order of the syllables within the sequence is unimportant for context. Specifically, sequences are composed of slightly modified syllables, thus increasing the probability of context-specificity. We note that future behavioral, e.g., playback experiments are needed in order to validate the biological relevance of our statistical results. We hypothesize that such sequences might have served as pre-syntax precursors in the evolution of animal communication.

Echolocating bats prefer a high risk-high gain foraging strategy to increase prey profitability.

Predators that target multiple prey types are predicted to switch foraging modes according to prey profitability to increase energy returns in dynamic environments. Here, we use bat-borne tags and DNA metabarcoding of feces to test the hypothesis that greater mouse-eared bats make immediate foraging decisions based on prey profitability and changes in the environment. We show that these bats use two foraging strategies with similar average nightly captures of 25 small, aerial insects and 29 large, ground-dwelling insects per bat, but with much higher capture success in the air (76%) vs ground (30%). However, owing to the 3-20 times larger ground prey, 85% of the nightly food acquisition comes from ground prey despite the 2.5 times higher failure rates. We find that most bats use the same foraging strategy on a given night suggesting that bats adapt their hunting behavior to weather and ground conditions. We conclude that these bats use high risk-high gain gleaning of ground prey as a primary foraging tactic, but switch to aerial hunting when environmental changes reduce the profitability of ground prey, showing that prey switching matched to environmental dynamics plays a key role in covering the energy intake even in specialized predators.

Bats are the only mammals capable of powered flight and therefore need a high calorie intake to survive. They hunt at night using the echoes made by their own calls to navigate and locate prey. Bats can use different tactics to hunt for food: hawking involves catching prey on the wing and requires fast aerial manoeuvring and more intense echolocation calls, while gleaning involves listening for movements of ground and water dwelling prey as the bat hovers. Some bat species specialise as hawkers or gleaners but maintain the ability to hunt with both methods. With the ever-growing impact of human activities on their habitats, it is important to understand how adaptable bats feeding habits are to changes in their environment. To find out more, Stidsholt et al. studied greater mouse-eared bats, which primarily feed by gleaning. To understand how this species chooses feeding strategies they fitted bats with tiny backpacks that could record the animal's location and foraging behaviour. They could also monitor prey sizes by recording the sounds of the bats chewing. Stidsholt et al. found that, although these bats tried to catch prey on the ground more often than in the air, they were actually more successful as airborne hunters. Despite this, gleaning was still a more profitable strategy for them, because the body mass of ground prey is higher than for airborne prey. Gleaning gave the bats a higher calorie intake, even though their capture rate was lower. Although feeding habits differed slightly between individual bats on a given night of monitoring, there were much larger changes in behaviour between different feeding nights. This shows that, although this species of bat prefers gleaning, they will switch strategies to hawking as their environment changes, for example if there is more airborne prey, or if rainfall makes it hard to hear movements on the ground. Bats tended to get enough calories for their needs but did not catch more prey than they needed to survive. Stidsholt et al. concluded that greater mouse-eared bats change their feeding strategy based on prey availability and size, as well as the bat's environment. Their study provides an important insight into how bats fit into the ecosystem and how adaptable bats might be to changes in their habitat.

In sickness and in health: the dynamics of the fruit bat gut microbiota under a bacterial antigen challenge and its association with the immune response.

Introduction: Interactions between the gut microbiome (GM) and the immune system influence host health and fitness. However, few studies have investigated this link and GM dynamics during disease in wild species. Bats (Mammalia: Chiroptera) have an exceptional ability to cope with intracellular pathogens and a unique GM adapted to powered flight. Yet, the contribution of the GM to bat health, especially immunity, or how it is affected by disease, remains unknown. Methods: Here, we examined the dynamics of the Egyptian fruit bats' (Rousettus aegyptiacus) GM during health and disease. We provoked an inflammatory response in bats using lipopolysaccharides (LPS), an endotoxin of Gram-negative bacteria. We then measured the inflammatory marker haptoglobin, a major acute phase protein in bats, and analyzed the GM (anal swabs) of control and challenged bats using high-throughput 16S rRNA sequencing, before the challenge, 24h and 48h post challenge. Results: We revealed that the antigen challenge causes a shift in the composition of the bat GM (e.g., Weissella, Escherichia, Streptococcus). This shift was significantly correlated with haptoglobin concentration, but more strongly with sampling time. Eleven bacterial sequences were correlated with haptoglobin concentration and nine were found to be potential predictors of the strength of the immune response, and implicit of infection severity, notably Weissella and Escherichia. The bat GM showed high resilience, regaining the colony's group GM composition rapidly, as bats resumed foraging and social activities. Conclusion: Our results demonstrate a tight link between bat immune response and changes in their GM, and emphasize the importance of integrating microbial ecology in ecoimmunological studies of wild species. The resilience of the GM may provide this species with an adaptive advantage to cope with infections and maintain colony health.

Bats experience age-related hearing loss (presbycusis).

Hearing loss is a hallmark of aging, typically initially affecting the higher frequencies. In echolocating bats, the ability to discern high frequencies is essential. However, nothing is known about age-related hearing loss in bats, and they are often assumed to be immune to it. We tested the hearing of 47 wild Egyptian fruit bats by recording their auditory brainstem response and cochlear microphonics, and we also assessed the cochlear histology in four of these bats. We used the bats' DNA methylation profile to evaluate their age and found that bats exhibit age-related hearing loss, with more prominent deterioration at the higher frequencies. The rate of the deterioration was ∼1 dB per year, comparable to the hearing loss observed in humans. Assessing the noise in the fruit bat roost revealed that these bats are exposed to continuous immense noise-mostly of social vocalizations-supporting the assumption that bats might be partially resistant to loud noise. Thus, in contrast to previous assumptions, our results suggest that bats constitute a model animal for the study of age-related hearing loss.

Sounds emitted by plants under stress are airborne and informative.

Stressed plants show altered phenotypes, including changes in color, smell, and shape. Yet, airborne sounds emitted by stressed plants have not been investigated before. Here we show that stressed plants emit airborne sounds that can be recorded from a distance and classified. We recorded ultrasonic sounds emitted by tomato and tobacco plants inside an acoustic chamber, and in a greenhouse, while monitoring the plant's physiological parameters. We developed machine learning models that succeeded in identifying the condition of the plants, including dehydration level and injury, based solely on the emitted sounds. These informative sounds may also be detectable by other organisms. This work opens avenues for understanding plants and their interactions with the environment and may have significant impact on agriculture.

Pregnancy-related sensory deficits might impair foraging in echolocating bats.

BACKGROUND: Reproduction entails substantial demands throughout its distinct stages. The mammalian gestation period imposes various energetic costs and movement deficits, but its effects on the sensory system are poorly understood. Bats rely heavily on active sensing, using echolocation to forage in complete darkness, or when lighting is uncertain. We examined the effects of pregnancy on bat echolocation. RESULTS: We show that pregnant Kuhl's pipistrelles (Pipistrellus kuhlii) altered their echolocation and flight behavior. Specifically, pregnant bats emitted longer echolocation signals at an ~ 15% lower rate, while flying more slowly and at a lower altitude compared to post-lactating females. A sensorimotor foraging model suggests that these changes could lead to an ~ 15% reduction in hunting performance during pregnancy. CONCLUSIONS: Sensory deficits related to pregnancy could impair foraging in echolocating bats. Our study demonstrates an additional cost of reproduction of possible relevance to other sensory modalities and organisms.

Echolocating bats rapidly adjust their mouth gape to control spatial acquisition when scanning a target.

BACKGROUND: As well known to any photographer, controlling the "field of view" offers an extremely powerful mechanism by which to adjust target acquisition. Only a few natural sensory systems can actively control their field of view (e.g., dolphins, whales, and bats). Bats are known for their active sensing abilities and modify their echolocation signals by actively controlling their spectral and temporal characteristics. Less is known about bats' ability to actively modify their bio-sonar field of view. RESULTS: We show that Pipistrellus kuhlii bats rapidly narrow their sensory field of view (i.e., their bio-sonar beam) when scanning a target. On-target vertical sonar beams were twofold narrower than off-target beams. Continuous measurements of the mouth gape of free-flying bats revealed that they control their bio-sonar beam by a ~3.6 mm widening of their mouth gape: namely, bats open their mouth to narrow the beam and vice versa. CONCLUSIONS: Bats actively and rapidly control their echolocation vertical beam width by modifying their mouth gape. We hypothesize that narrowing their vertical beam narrows the zone of ensonification when estimating the elevation of a target. In other words, bats open their mouth to improve sensory localization.

An artificial neural network explains how bats might use vision for navigation.

Animals navigate using various sensory information to guide their movement. Miniature tracking devices now allow documenting animals' routes with high accuracy. Despite this detailed description of animal movement, how animals translate sensory information to movement is poorly understood. Recent machine learning advances now allow addressing this question with unprecedented statistical learning tools. We harnessed this power to address visual-based navigation in fruit bats. We used machine learning and trained a convolutional neural network to navigate along a bat's route using visual information that would have been available to the real bat, which we collected using a drone. We show that a simple feed-forward network can learn to guide the agent towards a goal based on sensory input, and can generalize its learning both in time and in space. Our analysis suggests how animals could potentially use visual input for navigation and which features might be useful for this purpose.

A connectomics-based taxonomy of mammals.

Mammalian taxonomies are conventionally defined by morphological traits and genetics. How species differ in terms of neural circuits and whether inter-species differences in neural circuit organization conform to these taxonomies is unknown. The main obstacle to the comparison of neural architectures has been differences in network reconstruction techniques, yielding species-specific connectomes that are not directly comparable to one another. Here, we comprehensively chart connectome organization across the mammalian phylogenetic spectrum using a common reconstruction protocol. We analyse the mammalian MRI (MaMI) data set, a database that encompasses high-resolution ex vivo structural and diffusion MRI scans of 124 species across 12 taxonomic orders and 5 superorders, collected using a unified MRI protocol. We assess similarity between species connectomes using two methods: similarity of Laplacian eigenspectra and similarity of multiscale topological features. We find greater inter-species similarities among species within the same taxonomic order, suggesting that connectome organization reflects established taxonomic relationships defined by morphology and genetics. While all connectomes retain hallmark global features and relative proportions of connection classes, inter-species variation is driven by local regional connectivity profiles. By encoding connectomes into a common frame of reference, these findings establish a foundation for investigating how neural circuits change over phylogeny, forging a link from genes to circuits to behaviour.

Seasonal challenges of tropical bats in temperate zones.

To examine the challenges faced by free-ranging Rousettus aegyptiacus living at the northern edge of their distribution, we performed a retrospective analysis of 2196 clinical cases reported by a bat rescue NGO over a period of 36 months, from throughout Israel. All cases of injured bats were evaluated and categorized according to date, place, sex, age, and etiology of the morbidity. The data analysis revealed an increase in all types of morbidity during the wintertime, with more than two-fold the number of cases per week compared to in the summer, over three consecutive years. Moreover, we found that the number of abandoned pups peaked during spring and summer, when adult morbidity is minimal. We characterized two prominent types of previously undescribed morbidities in R. aegyptiacus. We also employed GPS tracking to monitor the movement and foraging of dozens of bats, and to examine the potential correlates of elevated winter morbidity. Our results suggest that it is mainly harsh weather that drives the observed winter morbidity, with food limitations playing a minor-role. We hypothesize that R. aegyptiacus, of tropical origin, is facing major seasonal survival difficulties near the northern edge of its distribution, probably limiting its spread further northwards still.

Revising the paradigm: Are bats really pathogen reservoirs or do they possess an efficient immune system?

While bats are often referred to as reservoirs of viral pathogens, a meta-analysis of the literature reveals many cases in which there is not enough evidence to claim so. In many cases, bats are able to confront viruses, recover, and remain immune by developing a potent titer of antibodies, often without becoming a reservoir. In other cases, bats might have carried an ancestral virus that at some time point might have mutated into a human pathogen. Moreover, bats exhibit a balanced immune response against viruses that have evolved over millions of years. Using genomic tools, it is now possible to obtain a deeper understanding of that unique immune system and its variability across the order Chiroptera. We conclude, that with the exception of a few viruses, bats pose little zoonotic danger to humans and that they operate a highly efficient anti-inflammatory response that we should strive to understand.

TrackUSF, a novel tool for automated ultrasonic vocalization analysis, reveals modified calls in a rat model of autism.

BACKGROUND: Various mammalian species emit ultrasonic vocalizations (USVs), which reflect their emotional state and mediate social interactions. USVs are usually analyzed by manual or semi-automated methodologies that categorize discrete USVs according to their structure in the frequency-time domains. This laborious analysis hinders the effective use of USVs as a readout for high-throughput analysis of behavioral changes in animals. RESULTS: Here we present a novel automated open-source tool that utilizes a different approach towards USV analysis, termed TrackUSF. To validate TrackUSF, we analyzed calls from different animal species, namely mice, rats, and bats, recorded in various settings and compared the results with a manual analysis by a trained observer. We found that TrackUSF detected the majority of USVs, with less than 1% of false-positive detections. We then employed TrackUSF to analyze social vocalizations in Shank3-deficient rats, a rat model of autism, and revealed that these vocalizations exhibit a spectrum of deviations from appetitive calls towards aversive calls. CONCLUSIONS: TrackUSF is a simple and easy-to-use system that may be used for a high-throughput comparison of ultrasonic vocalizations between groups of animals of any kind in any setting, with no prior assumptions.

Alone, in the dark: The extraordinary neuroethology of the solitary blind mole rat.

On the social scale, the blind mole rat (BMR; Spalax ehrenbergi) is an extreme. It is exceedingly solitary, territorial, and aggressive. BMRs reside underground, in self-excavated tunnels that they rarely leave. They possess specialized sensory systems for social communication and navigation, which allow them to cope with the harsh environmental conditions underground. This review aims to present the blind mole rat as an ideal, novel neuroethological model for studying aggressive and solitary behaviors. We discuss the BMR's unique behavioral phenotype, particularly in the context of 'anti-social' behaviors, and review the available literature regarding its specialized sensory adaptations to the social and physical habitat. To date, the neurobiology of the blind mole rat remains mostly unknown and holds a promising avenue for scientific discovery. Unraveling the neural basis of the BMR's behavior, in comparison to that of social rodents, can shed important light on the underlying mechanisms of psychiatric disorders in humans, in which similar behaviors are displayed.