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.

By a whisker: the sensory role of vibrissae in hovering flight in nectarivorous bats.

Whiskers are important tactile structures widely used across mammals for a variety of sensory functions, but it is not known how bats-representing about a fifth of all extant mammal species-use them. Nectar-eating bats typically have long vibrissae (long, stiff hairs) arranged in a forward-facing brush-like formation that is not present in most non-nectarivorous bats. They also commonly use a unique flight strategy to access their food-hovering flight. Here we investigated whether these species use their vibrissae to optimize their feeding by assisting fine flight control. We used behavioural experiments to test if bats' flight trajectory into the flower changed after vibrissa removal, and phylogenetic comparative methods to test whether vibrissa length is related to nectarivory. We found that bat flight trajectory was altered after vibrissae removal and that nectarivorous bats possess longer vibrissae than non-nectivorous species, providing evidence of an additional source of information in bats' diverse sensory toolkit.

Thinking small: Next-generation sensor networks close the size gap in vertebrate biologging.

Recent advances in animal tracking technology have ushered in a new era in biologging. However, the considerable size of many sophisticated biologging devices restricts their application to larger animals, whereas older techniques often still represent the state-of-the-art for studying small vertebrates. In industrial applications, low-power wireless sensor networks (WSNs) fulfill requirements similar to those needed to monitor animal behavior at high resolution and at low tag mass. We developed a wireless biologging network (WBN), which enables simultaneous direct proximity sensing, high-resolution tracking, and long-range remote data download at tag masses of 1 to 2 g. Deployments to study wild bats created social networks and flight trajectories of unprecedented quality. Our developments highlight the vast capabilities of WBNs and their potential to close an important gap in biologging: fully automated tracking and proximity sensing of small animals, even in closed habitats, at high spatial and temporal resolution.

Mammalian deltavirus without hepadnavirus coinfection in the neotropical rodent Proechimys semispinosus.

Hepatitis delta virus (HDV) is a human hepatitis-causing RNA virus, unrelated to any other taxonomic group of RNA viruses. Its occurrence as a satellite virus of hepatitis B virus (HBV) is a singular case in animal virology for which no consensus evolutionary explanation exists. Here we present a mammalian deltavirus that does not occur in humans, identified in the neotropical rodent species Proechimys semispinosus The rodent deltavirus is highly distinct, showing a common ancestor with a recently described deltavirus in snakes. Reverse genetics based on a tandem minus-strand complementary DNA genome copy under the control of a cytomegalovirus (CMV) promoter confirms autonomous genome replication in transfected cells, with initiation of replication from the upstream genome copy. In contrast to HDV, a large delta antigen is not expressed and the farnesylation motif critical for HBV interaction is absent from a genome region that might correspond to a hypothetical rodent large delta antigen. Correspondingly, there is no evidence for coinfection with an HBV-related hepadnavirus based on virus detection and serology in any deltavirus-positive animal. No other coinfecting viruses were detected by RNA sequencing studies of 120 wild-caught animals that could serve as a potential helper virus. The presence of virus in blood and pronounced detection in reproductively active males suggest horizontal transmission linked to competitive behavior. Our study establishes a nonhuman, mammalian deltavirus that occurs as a horizontally transmitted infection, is potentially cleared by immune response, is not focused in the liver, and possibly does not require helper virus coinfection.

Cross-modal facilitation of auditory discrimination in a frog.

Stimulation in one sensory modality can affect perception in a separate modality, resulting in diverse effects including illusions in humans. This can also result in cross-modal facilitation, a process where sensory performance in one modality is improved by stimulation in another modality. For instance, a simple sound can improve performance in a visual task in both humans and cats. However, the range of contexts and underlying mechanisms that evoke such facilitation effects remain poorly understood. Here, we demonstrated cross-modal stimulation in wild-caught túngara frogs, a species with well-studied acoustic preferences in females. We first identified that a combined visual and seismic cue (vocal sac movement and water ripple) was behaviourally relevant for females choosing between two courtship calls in a phonotaxis assay. We then found that this combined cross-modal stimulus rescued a species-typical acoustic preference in the presence of background noise that otherwise abolished the preference. These results highlight how cross-modal stimulation can prime attention in receivers to improve performance during decision-making. With this, we provide the foundation for future work uncovering the processes and conditions that promote cross-modal facilitation effects.

Covariation among multimodal components in the courtship display of the túngara frog.

Communication systems often include a variety of components, including those that span modalities, which may facilitate detection and decision-making. For example, female túngara frogs and fringe-lipped bats generally rely on acoustic mating signals to find male túngara frogs in a mating or foraging context, respectively. However, two additional cues (vocal sac inflation and water ripples) can enhance detection and choice behavior. To date, we do not know the natural variation and covariation of these three components. To address this, we made detailed recordings of calling males, including call amplitude, vocal sac volume and water ripple height, in 54 frogs (2430 calls). We found that all three measures correlated, with the strongest association between the vocal sac volume and call amplitude. We also found that multimodal models predicted the mass of calling males better than unimodal models. These results demonstrate how multimodal components of a communication system relate to each other and provide an important foundation for future studies on how receivers integrate and compare complex displays.

Complex sensory environments alter mate choice outcomes.

Noise is a common problem in animal communication. We know little, however, about how animals communicate in the presence of noise using multimodal signals. Multimodal signals are hypothesised to be favoured by evolution because they increase the efficacy of detection and discrimination in noisy environments. We tested the hypothesis that female túngara frogs' responses to attractive male advertisement calls are improved in noise when a visual signal component is added to the available choices. We tested this at two levels of decision complexity (two and three choices). In a two-choice test, the presence of noise did not reduce female preferences for attractive calls. The visual component of a calling male, associated with an unattractive call, also did not reduce preference for attractive calls in the absence of noise. In the presence of noise, however, females were more likely to choose an unattractive call coupled with the visual component. In three-choice tests, the presence of noise alone reduced female responses to attractive calls and this was not strongly affected by the presence or absence of visual components. The responses in these experiments fail to support the multimodal signal efficacy hypothesis. Instead, the data suggest that audio-visual perception and cognitive processing, related to mate choice decisions, are dependent on the complexity of the sensory scene.

Flying bats use serial sampling to locate odour sources.

Olfactory tracking generally sacrifices speed for sensitivity, but some fast-moving animals appear surprisingly efficient at foraging by smell. Here, we analysed the olfactory tracking strategies of flying bats foraging for fruit. Fruit- and nectar-feeding bats use odour cues to find food despite the sensory challenges derived from fast flight speeds and echolocation. We trained Jamaican fruit-eating bats (Artibeus jamaicensis) to locate an odour reward and reconstructed their flight paths in three-dimensional space. Results confirmed that bats relied upon olfactory cues to locate a reward. Flight paths revealed a combination of odour- and memory-guided search strategies. During 'inspection flights', bats significantly reduced flight speeds and flew within approximately 6 cm of possible targets to evaluate the presence or absence of the odour cue. This behaviour combined with echolocation explains how bats maximize foraging efficiency while compensating for trade-offs associated with olfactory detection and locomotion.

Agua Salud alphavirus defines a novel lineage of insect-specific alphaviruses discovered in the New World.

The genus Alphavirus harbours mostly insect-transmitted viruses that cause severe disease in humans, livestock and wildlife. Thus far, only three alphaviruses with a host range restricted to insects have been found in mosquitoes from the Old World, namely Eilat virus (EILV), Taï Forest alphavirus (TALV) and Mwinilunga alphavirus (MWAV). In this study, we found a novel alphavirus in one Culex declarator mosquito sampled in Panama. The virus was isolated in C6/36 mosquito cells, and full genome sequencing revealed an 11 468 nt long genome with maximum pairwise nucleotide identity of 62.7 % to Sindbis virus. Phylogenetic analyses placed the virus as a solitary deep rooting lineage in a basal relationship to the Western equine encephalitis antigenic complex and to the clade comprising EILV, TALV and MWAV, indicating the detection of a novel alphavirus, tentatively named Agua Salud alphavirus (ASALV). No growth of ASALV was detected in vertebrate cell lines, including cell lines derived from ectothermic animals, and replication of ASALV was strongly impaired above 31 °C, suggesting that ASALV represents the first insect-restricted alphavirus of the New World.

Sickness effects on social interactions depend on the type of behaviour and relationship.

Infections can change social behaviour in multiple ways, with profound impacts on pathogen transmission. However, these impacts might depend on the type of behaviour, how sociality as a biological trait is defined (e.g. network degree vs. mean edge strength) and the type of social relationship between the interacting individuals. We used the highly social common vampire bat Desmodus rotundus to test how an immune challenge by lipopolysaccharide (LPS) injections affects two different social behaviours and three alternate measures of sociality, and whether the LPS effect differs by kinship relationship. Effects of sickness should be lower for social behaviours that bestow greater benefits to inclusive fitness, such as food sharing. As predicted, immune-challenged bats experienced a greater reduction in allogrooming received than food sharing received. Sickness effects might also depend on how a social interaction is defined (e.g. the number of grooming partners vs. the duration of grooming events). We predicted that sickness would impact both the number and duration of social encounters, but we only detected a decrease in the number of grooming partners. Finally, sickness effects might vary with social relationship type. We predicted that sickness effects should be smaller for interactions among close kin. As expected, the immune challenge had smaller effects on mother-offspring interactions. In conclusion, our results highlight the need to explicitly consider how the effects of sickness on social network structure can differ depending on the 'who, what, and how' of social interactions, because these factors are likely to influence how sickness behaviour alters pathogen transmission.

Immune-challenged vampire bats produce fewer contact calls.

Vocalizations are an important means to facilitate social interactions, but vocal communication may be affected by infections. While such effects have been shown for mate-attraction calls, other vocalizations that facilitate social contact have received less attention. When isolated, vampire bats produce contact calls that attract highly associated groupmates. Here, we test the effect of an immune challenge on contact calling rates of individually isolated vampire bats. Sickness behaviour did not appear to change call structure, but it decreased the number of contact calls produced. This effect could decrease contact with groupmates and augment other established mechanisms by which sickness reduces social encounters (e.g. mortality, lethargy and social withdrawal or disinterest).

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.

Diverse novel phleboviruses in sandflies from the Panama Canal area, Central Panama.

The genus Phlebovirus (order Bunyavirales, family Phenuiviridae) comprises 57 viruses that are grouped into nine species-complexes. Sandfly-transmitted phleboviruses are found in Europe, Africa and the Americas and are responsible for febrile illness and infections of the nervous system in humans. The aim of this study was to assess the genetic diversity of sandfly-transmitted phleboviruses in connected and isolated forest habitats throughout the Panama Canal area in Central Panama. In total, we collected 13 807 sandflies comprising eight phlebotomine species. We detected several strains pertaining to five previously unknown viruses showing maximum pairwise identities of 45-78 % to the RNA-dependent RNA polymerase genes of phleboviruses. Entire coding regions were directly sequenced from infected sandflies as virus isolation in cell culture was not successful. The viruses were tentatively named La Gloria virus (LAGV), Mona Grita virus (MOGV), Peña Blanca virus (PEBV), Tico virus (TICV) and Tres Almendras virus (TRAV). Inferred phylogenies and p-distance-based analyses revealed that PEBV groups with the Bujaru phlebovirus species-complex, TRAV with the Candiru phlebovirus species-complex and MOGV belongs to the proposed Icoarci phlebovirus species-complex, whereas LAGV and TICV seem to be distant members of the Bujaru phlebovirus species-complex. No specific vector or habitat association was found for any of the five viruses. Relative abundance of sandflies was similar over habitat types. Our study shows that blood-feeding insects originating from remote and biodiverse habitats harbour multiple previously unknown phleboviruses. These viruses should be included in future surveillance studies to assess their geographic distribution and to elucidate if these viruses cause symptoms of disease in animals or humans.

Synchronized mating signals in a communication network: the challenge of avoiding predators while attracting mates.

Conspicuous mating signals attract mates but also expose signallers to predators and parasites. Signal evolution, therefore, is driven by conflicting selective pressures from multiple receivers, both target and non-target. Synchronization of mating signals, for example, is an evolutionary puzzle, given the assumed high cost of reduced female attraction when signals overlap. Synchronization may be beneficial, however, if overlapping signals reduce attraction of non-target receivers. We investigate how signal synchronization is shaped by the trade-off between natural and sexual selection in two anuran species: pug-nosed tree frogs (Smilisca sila), in which males produce mating calls in near-perfect synchrony, and túngara frogs (Engystomops pustulosus), in which males alternate their calls. To examine the trade-off imposed by signal synchronization, we conducted field and laboratory playback experiments on eavesdropping enemies (bats and midges) and target receivers (female frogs). Our results suggest that, while synchronization can be a general strategy for signallers to reduce their exposure to eavesdroppers, relaxed selection by females for unsynchronized calls is key to the evolution and maintenance of signal synchrony. This study highlights the role of relaxed selection in our understanding of the origin of mating signals and displays.

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.

Exploratory behavior of a native anuran species with high invasive potential.

Exploratory behavior can be a key component of survival in novel or changing environments, ultimately determining population establishment. While many studies have investigated the behavior of wild animals in response to novel food items or objects, our understanding of how they explore novel environments is limited. Here, we examine how experience affects the foraging behavior of a species with high invasive potential. In particular, we investigate the movement and behavior of cane toads as a function of experience in a novel environment, and how the presence of food modulates exploration. Cane toads, from a population in their native range, were repeatedly tested in a large, naturalistic arena with or without food present. Both groups exhibited significant but different changes in exploratory behavior. While toads in an environment without food reduced exploratory behavior over trials, those with food present increased both food intake per trial and the directness of their paths to food, resulting in fewer approaches to food patches over time. Our results suggest that cane toads learn patch location and provide preliminary evidence suggesting toads use spatial memory, not associative learning, to locate food. In sum, we show that with experience, cane toads alter their behavior to increase foraging efficiency. This study emphasizes the role of learning in foraging in cane toads, a characteristic that may have facilitated their success as invaders.

Ecological drivers of Hepacivirus infection in a neotropical rodent inhabiting landscapes with various degrees of human environmental change.

Anthropogenic environmental change can impact community and population traits such as species diversity and population densities, which have been shown to influence the prevalence of viruses in wildlife reservoirs. In particular, host species resilient to changes in their natural habitat may increase in numbers, which in turn can affect the prevalence of directly transmitted viruses. We have carried out a survey of small mammal communities in three tropical landscapes differing in their degree of environmental change in Central Panama and investigated the effects of community changes on Hepacivirus prevalence. The modification of continuous habitat into partly connected or isolated habitat patches during the past century was linked to changes in species diversity and species assemblages, which was further associated with shifts in the abundance of generalist marsupial (Didelphis marsupialis, Philander opossum) and rodent (Proechimys semispinosus) species. The latter has become dominant in isolated habitat patches and was the only identified Hepacivirus host in our study system. Our analyses suggest that, in addition to the effects of host age and sex, host population density in interaction with sex ratio is a crucial predictor of infection probability. Although we found no significant relationships between species diversity per se and infection probability, the lowest prevalence detected in the landscape with the highest species diversity indicates that shifts in species assemblages (e.g. changes in the presence and abundance of marsupial predators) impact the host's intraspecific contact rates, the probability of virus transmission and, thus, the virus prevalence. Our study additionally provides important data on the influence of human-induced landscape changes on infection probability and, therefore, on virus prevalence in wildlife and emphasizes the importance of a landscape-scale approach with concomitant consideration of the complex interactions between ecological factors.

Leg structure explains host site preference in bat flies (Diptera: Streblidae) parasitizing neotropical bats (Chiroptera: Phyllostomidae).

Bat flies (Streblidae) are diverse, obligate blood-feeding insects and probably the most conspicuous ectoparasites of bats. They show preferences for specific body regions on their host bat, which are reflected in behavioural characteristics. In this study, we corroborate the categorization of bat flies into three ecomorphological groups, focusing only on differences in hind leg morphology. As no detailed phylogeny of bat flies is available, it remains uncertain whether these morphological differences reflect the evolutionary history of bat flies or show convergent adaptations for the host habitat type. We show that the division of the host bat into three distinct habitats contributes to the avoidance of interspecific competition of bat fly species. Finally, we found evidence for density-dependent competition between species belonging to the same ecomorphological group.

Seeds of HOPE: Incorporating Community-Based Strategies to Implement a Weight-Loss and Empowerment Intervention in Eastern North Carolina.

Seeds of HOPE (Health, Opportunities, Partnerships, and Empowerment) was a community-based participatory research project designed to implement an evidence-based weight loss and empowerment intervention aimed at increasing self-efficacy through peer support. HOPE Works, its model, has yielded significant weight loss and increases in participants' ability to set and achieve goals, including in consumption of fruits and vegetables and in physical activity.METHODS The Seeds of HOPE project was implemented through 3 peer leader recruitment approaches using Circle Leaders. Study participants met in hope circles to discuss various topics aimed at developing healthier lifestyles. Changes at 6-month intervals were assessed in health behaviors, weight, and hope. One-way ANOVA was used to test differences in mean change in weight and hope across the 3 recruitment approaches.RESULTS Study participants (N = 146) lost weight (-3.3 pounds, P = 0.003, 95% CI: -5.40 - -1.27). Fruit consumption significantly increased (P = 0.04, 95% CI: 0.01-0.41) while no changes in vegetable consumption or physical activity were observed. No differences based on different leader recruitment approaches were found.LIMITATIONS There were limitations in the power to fully detect differences across Circle Leader recruitment approaches; loss-to-follow up and representativeness of the sample were present. Further research is needed to determine if these approaches would be successful in other rural counties, with different genders, or with individuals in urban and/or higher socioeconomic populations.CONCLUSIONS Participants found modest success in weight loss and fruit consumption. Authors find that community engagement strategies are helpful in finding mutually acceptable adaptations to implement interventions such as Seeds of HOPE in diverse communities.