If a bird flies in the forest,does an insect hear it?

Birds are major predators of many eared insects including moths, butterflies, crickets and cicadas. We provide evidence supporting the hypothesis that insect ears can function as ‘bird detectors’. First, we show that birds produce flight sounds while foraging. Eastern phoebes (Sayornis phoebe) and chickadees (Poecile atricapillus) generate broadband sounds composed of distinct repetitive elements (approx. 18 and 20 Hz, respectively) that correspond to cyclic wing beating. We estimate that insects can detect an approaching bird from distances of at least 2.5 m, based on insect hearing thresholds and sound level measurements of bird flight. Second, we show that insects with both high and low frequency hearing can hear bird flight sounds. Auditory nerve cells of noctuid moths (Trichoplusia ni) and nymphalid butterflies (Morpho peleides) responded in a bursting pattern to playbacks of an attacking bird. This is the first study to demonstrate that foraging birds generate flight sound cues that are detectable by eared insects. Whether insects exploit these sound cues, and alternatively, if birds have evolved sound-reducing foraging tactics to render them acoustically ‘cryptic’ to their prey, are tantalizing questions worthy of further investigation.     

Your attention please: increasing ambient noise levels elicits a change in communication behaviour in humpback whales (Megaptera novaeangliae)

High background noise is an important obstacle in successful signal detection and perception of an intended acoustic signal. To overcome this problem, many animals modify their acoustic signal by increasing the repetition rate, duration, amplitude or frequency range of the signal. An alternative method to ensure successful signal reception, yet to be tested in animals, involves the use of two different types of signal, where one signal type may enhance the other in periods of high background noise. Humpback whale communication signals comprise two different types: vocal signals, and surface-generated signals such as ‘breaching’ or ‘pectoral slapping’. We found that humpback whales gradually switched from primarily vocal to primarily surface-generated communication in increasing wind speeds and background noise levels, though kept both signal types in their repertoire. Vocal signals have the advantage of having higher information content but may have the disadvantage of loosing this information in a noisy environment. Surface-generated sounds have energy distributed over a greater frequency range and may be less likely to become confused in periods of high wind-generated noise but have less information content when compared with vocal sounds. Therefore, surface-generated sounds may improve detection or enhance the perception of vocal signals in a noisy environment.     

Social calls used by a leaf-roosting bat to signal location

Social calls in bats have many functions, including mate attraction and maintaining contact during flight. Research suggests that social calls may also be used to transfer information about roosts, but no studies have yet demonstrated that calls are used to actively attract conspecifics to roosting locations. We document the social calls used by Spix''s disc-winged bat (Thyroptera tricolor) to actively recruit group members to roosts. In acoustic trials, we recorded two sets of calls; one from flying individuals termed ‘inquiry calls’, and another from roosting bats termed ‘response calls’. Inquiry calls were emitted by flying bats immediately upon release, and quickly (i.e. 178 ms) elicited production of response calls from roosting individuals. Most flying bats entered the roost when roosting individuals responded, while few bats entered the roost in the absence of a response. We argue that information transfer concerning roost location may facilitate sociality in T. tricolor, given the ephemeral nature of roosting structures used by this species.     

Male dance moves that catch a woman's eye

Male movements serve as courtship signals in many animal species, and may honestly reflect the genotypic and/or phenotypic quality of the individual. Attractive human dance moves, particularly those of males, have been reported to show associations with measures of physical strength, prenatal androgenization and symmetry. Here we use advanced three-dimensional motion-capture technology to identify possible biomechanical differences between women''s perceptions of ‘good’ and ‘bad’ male dancers. Nineteen males were recorded using the ‘Vicon’ motion-capture system while dancing to a basic rhythm; controlled stimuli in the form of avatars were then created in the form of 15 s video clips, and rated by 39 females for dance quality. Initial analyses showed that 11 movement variables were significantly positively correlated with perceived dance quality. Linear regression subsequently revealed that three movement measures were key predictors of dance quality; these were variability and amplitude of movements of the neck and trunk, and speed of movements of the right knee. In summary, we have identified specific movements within men''s dance that influence women''s perceptions of dancing ability. We suggest that such movements may form honest signals of male quality in terms of health, vigour or strength, though this remains to be confirmed.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

Costly major histocompatibility complex signals produced only by reproductively active males,but not females,must be validated by a ‘maleness signal’ in three-spined sticklebacks

Olfactory information about individual major histocompatibility complex (MHC) immune genotypes is important for mate choice in several species. For example, during the mate choice decisions of three-spined sticklebacks, females assess males on the basis of odour cues that convey information about their MHC diversity. Here, we show that an additional ‘maleness’ signal is needed to validate the MHC signal. Furthermore, using interaction between natural odour of sticklebacks and synthetic MHC-ligand peptides, we show that MHC signals are conditional on the reproductive state in males. By contrast, we find that gravid females do not produce such signals. Since MHC olfactory signals relevant to mate choice decisions are conditional upon gender and reproductive state, we suggest that their manufacture is likely to be costly to senders, and therefore, potentially conditional on the health/parasitization status of the sender. We hypothesize that shedding of peptide–MHC complexes compromises immune function, selecting against unconditional use of these signals.     

Odour cues from suitors’ nests determine mating success in a fish

Animals use a range of sensory cues for finding food, avoiding predators and choosing mates. In this regard, the aquatic environment is particularly suitable for the use of olfactory and other chemical cues. Nevertheless, mate choice research, even on aquatic organisms, has focused on visual signals, while chemical cues relevant in sexual selection have been assumed to be ‘intrinsic’ excretions of mate candidates. Here, using the sand goby Pomatoschistus minutus, a small fish with paternal egg care, we investigated the possibility that ‘extrinsic’ chemical cues in the males’ nests could also have a significant contribution to mating success. We found that females strongly avoided laying eggs into nests subject to the odour of Saprolegnia water moulds (an egg infection) and that this effect was independent of the females’ initial, visually based preference for males. To the best of our knowledge, this is the first study to show that chemical cues related to parental failure can play a large role in sexual selection.     

Strong behavioural defensive responses of endemic Rana latastei tadpoles induced by a native predator's odour

Prey species must constantly acquire information on predator identity, abundance and dangerousness from the environment. In aquatic habitats, this information is mainly propagated by water-borne chemical signals, either predator-specific odours or prey alarm cues. Anuran larvae innately respond to conspecific alarm cues and are able to associate them to predator cues during their lifetime. In this study, we investigated the anti-predatory responses of endemic Italian agile frog (Rana latastei) tadpoles exposed to either conspecific or heterospecific alarm cues and a native predator's (Anax imperator larvae) odour. Pre-and post-stimulus behaviours of each tadpole were recorded by a digital camera and analysed by a source executable software for image-based tracking. We found that Italian agile frog tadpoles responded to fasted dragonfly odour by strongly reducing their activity, both in terms of the amount of time they spent active and path length covered in comparison to control groups. Contrary to previous studies, predators' diet had a negligible effect on tadpole response and our experiment did not bring any evidence of the phylogenetic-relatedness hypothesis. The innate or early-in-development recognition of dragonfly larvae is clearly adaptive and may increase tadpole survival with relatively low costs, but, at the same time, may increase the risk of ignoring novel potential threats.     

Interspecific signalling between mutualists: food-thieving drongos use a cooperative sentinel call to manipulate foraging partners

Interspecific communication is common in nature, particularly between mutualists. However, whether signals evolved for communication with other species, or are in fact conspecific signals eavesdropped upon by partners, is often unclear. Fork-tailed drongos (Dicrurus adsimilis) associate with mixed-species groups and often produce true alarms at predators, whereupon associating species flee to cover, but also false alarms to steal associating species'' food (kleptoparasitism). Despite such deception, associating species respond to drongo non-alarm calls by increasing their foraging and decreasing vigilance. Yet, whether these calls represent interspecific sentinel signals remains unknown. We show that drongos produced a specific sentinel call when foraging with a common associate, the sociable weaver (Philetairus socius), but not when alone. Weavers increased their foraging and decreased vigilance when naturally associating with drongos, and in response to sentinel call playback. Further, drongos sentinel-called more often when weavers were moving, and weavers approached sentinel calls, suggesting a recruitment function. Finally, drongos sentinel-called when weavers fled following false alarms, thereby reducing disruption to weaver foraging time. Results therefore provide evidence of an ‘all clear’ signal that mitigates the cost of inaccurate communication. Our results suggest that drongos enhance exploitation of a foraging mutualist through coevolution of interspecific sentinel signals.     

Embryonic substances induce alarm response in adult zebrafish (Danio rerio)

Many aquatic animals rely on chemicals released by injured individuals of the same species to assess predation risk. Among these chemical cues, alarm substances released from the injured skin of ostariophysan fishes have been extensively examined. In most fish species examined, these cues appear to be released by all injured individuals (including larvae, juveniles and adults) and elicit alarm responses in conspecifics. Adult alarm cues also affect development and physiology of embryos. Nonetheless, whether embryos produce alarm cues that affect adults is not known. This study reports that extracts of zebrafish (Danio rerio) embryos at 36 h post-fertilization or later induce antipredator behaviours reminiscent of those induced by skin alarm substances. At an equivalent of 10⁻⁶ g embryo per millilitre, the extract induced bottom-dwelling and freezing in adults. These behaviours are consistent with those induced by adult alarm substances. This study concludes that zebrafish embryos produce alarm substances.     

Friends in Low Places: Responses of a Benthic Stream Fish to Intra‐Prey‐Guild Alarm Cues

Many aquatic species produce chemical alarm cues that serve as a warning to nearby conspecifics. In mixed‐species aggregations, individuals may also benefit by ‘eavesdropping’ on the chemical alarm cues of other species that are in the same prey guild. Rainbow Darters (Etheostoma caeruleum) are benthic fish that co‐occur with native Ozark Minnows (Notropis nubilus), recently introduced Western Mosquitofish (Gambusia affinis), and native Oklahoma Salamanders (Eurycea tyrnerensis), all of whom are vulnerable to the same predators. We tested the responses of darters to the damage‐released alarm cues of conspecifics (positive control), minnows, and mosquitofish; alarm cues from Bumblebee Gobies (Brachygobius doriae) served as a negative (allopatric) control. We also tested the response of sympatric and allopatric darters to the damage‐released alarm cues of Oklahoma Salamander. Darters exhibited a fright response to conspecific and minnow alarm cues, but not to cues from mosquitofish or gobies. Lack of response to mosquitofish cues could be because they are introduced or because they typically occur higher in the water column than darters. Darters that were sympatric with the salamander exhibited a fright response to the alarm cues of the salamander, while allopatric darters did not. Rainbow Darters can develop responses to the alarm cues of syntopic species (minnows and Oklahoma Salamander) within their prey guild.     

Further Explorations of the Facing Bias in Biological Motion Perception: Perspective Cues,Observer Sex,and Response Times

The human visual system has evolved to be highly sensitive to visual information about other persons and their movements as is illustrated by the effortless perception of point-light figures or ‘biological motion’. When presented orthographically, a point-light walker is interpreted in two anatomically plausible ways: As ‘facing the viewer’ or as ‘facing away’ from the viewer. However, human observers show a ‘facing bias’: They perceive such a point-light walker as facing towards them in about 70-80% of the cases. In studies exploring the role of social and biological relevance as a possible account for the facing bias, we found a ‘figure gender effect’: Male point-light figures elicit a stronger facing bias than female point-light figures. Moreover, we also found an ‘observer gender effect’: The ‘figure gender effect’ was stronger for male than for female observers. In the present study we presented to 11 males and 11 females point-light walkers of which, very subtly, the perspective information was manipulated by modifying the earlier reported ‘perspective technique’. Proportions of ‘facing the viewer’ responses and reaction times were recorded. Results show that human observers, even in the absence of local shape or size cues, easily pick up on perspective cues, confirming recent demonstrations of high visual sensitivity to cues on whether another person is potentially approaching. We also found a consistent difference in how male and female observers respond to stimulus variations (figure gender or perspective cues) that cause variations in the perceived in-depth orientation of a point-light walker. Thus, the ‘figure gender effect’ is possibly caused by changes in the relative locations and motions of the dots that the perceptual system tends to interpret as perspective cues. Third, reaction time measures confirmed the existence of the facing bias and recent research showing faster detection of approaching than receding biological motion.     

Eavesdropping on heterospecific alarm calls: from mechanisms to consequences

Animals often gather information from other species by eavesdropping on signals intended for others. We review the extent, benefits, mechanisms, and ecological and evolutionary consequences of eavesdropping on other species' alarm calls. Eavesdropping has been shown experimentally in about 70 vertebrate species, and can entail closely or distantly related species. The benefits of eavesdropping include prompting immediate anti‐predator responses, indirect enhancement of foraging or changed habitat use, and learning about predators. Eavesdropping on heterospecifics can provide more eyes looking for danger, complementary information to that from conspecifics, and potentially information at reduced cost. The response to heterospecific calls can be unlearned or learned. Unlearned responses occur when heterospecific calls have acoustic features similar to that used to recognize conspecific calls, or acoustic properties such as harsh sounds that prompt attention and may allow recognition or facilitate learning. Learning to recognize heterospecific alarm calls is probably essential to allow recognition of the diversity of alarm calls, but the evidence is largely indirect. The value of eavesdropping on different species is affected by problems of signal interception and the relevance of heterospecific alarm calls to the listener. These constraints on eavesdropping will affect how information flows among species and thus affect community function. Some species are ‘keystone’ information producers, while others largely seek information, and these differences probably affect the formation and function of mixed‐species groups. Eavesdroppers might also integrate alarm calls from multiple species to extract relevant and reliable information. Eavesdropping appears to set the stage for the evolution of interspecific deception and communication, and potentially affects communication within species. Overall, we now know that eavesdropping on heterospecific alarm calls is an important source of information for many species across the globe, and there are ample opportunities for research on mechanisms, fitness consequences and implications for community function and signalling evolution.     

Double meaning of courtship song in a moth

Males use courtship signals to inform a conspecific female of their presence and/or quality, or, alternatively, to ‘cheat’ females by imitating the cues of a prey or predator. These signals have the single function of advertising for mating. Here, we show the dual functions of the courtship song in the yellow peach moth, Conogethes punctiferalis, whose males generate a series of short pulses and a subsequent long pulse in a song bout. Repulsive short pulses mimic the echolocation calls of sympatric horseshoe bats and disrupt the approach of male rivals to a female. The attractive long pulse does not mimic bat calls and specifically induces mate acceptance in the female, who raises her wings to facilitate copulation. These results demonstrate that moths can evolve both attractive acoustic signals and repulsive ones from cues that were originally used to identify predators and non-predators, because the bat-like sounds disrupt rivals, and also support a hypothesis of signal evolution via receiver bias in moth acoustic communication that was driven by the initial evolution of hearing to perceive echolocating bat predators.     

First evidence of fish larvae producing sounds

The acoustic ecology of marine fishes has traditionally focused on adults, while overlooking the early life-history stages. Here, we document the first acoustic recordings of pre-settlement stage grey snapper larvae (Lutjanus griseus). Through a combination of in situ and unprovoked laboratory recordings, we found that L. griseus larvae are acoustically active during the night, producing ‘knock’ and ‘growl’ sounds that are spectrally and temporally similar to those of adults. While the exact function and physiological mechanisms of sound production in fish larvae are unknown, we suggest that these sounds may enable snapper larvae to maintain group cohesion at night when visual cues are reduced.     

A death in the family: Sea lamprey (Petromyzon marinus) avoidance of confamilial alarm cues diminishes with phylogenetic distance

Alarm signals released after predator attack function as reliable public information revealing areas of high risk. The utility of this information can extend beyond species boundaries, benefiting heterospecifics capable of recognizing and responding appropriately to the signal. Nonmutually exclusive hypotheses explaining the acquisition of heterospecific reactivity to cues suggest it could be conserved phylogenetically following its evolution in a common ancestor (a species‐level effect) and/or learned during periods of shared risk (a population‐level effect; e.g., shared predators). Using a laboratory‐based space‐use behavioral assay, we tested the response of sea lamprey (Petromyzon marinus) to the damage‐released alarm cues of five confamilial (sympatric and allopatric) species and two distantly related out‐groups: a sympatric teleost (white sucker Catostomus commersonii) and an allopatric agnathan (Atlantic hagfish Myxine glutinosa). We found that sea lamprey differed in their response to conspecific and heterospecific odors; exhibiting progressively weaker avoidance of cues derived from more phylogenetically distant confamilials regardless of current overlap in distribution. Odors from out‐groups elicited no response. These findings suggest that a damage‐released alarm cue is at least partially conserved within the Petromyzontidae and that sea lamprey perceives predator attacks directed to closely related taxa. These findings are consistent with similar observations from gastropod, amphibian and bony fish taxa, and we discuss this in an eco‐evo context to provide a plausible explanation for the acquisition and maintenance of the response in sea lamprey.     

Large-Scale Analysis of Auditory Segregation Behavior Crowdsourced via a Smartphone App

The human auditory system is adept at detecting sound sources of interest from a complex mixture of several other simultaneous sounds. The ability to selectively attend to the speech of one speaker whilst ignoring other speakers and background noise is of vital biological significance—the capacity to make sense of complex ‘auditory scenes’ is significantly impaired in aging populations as well as those with hearing loss. We investigated this problem by designing a synthetic signal, termed the ‘stochastic figure-ground’ stimulus that captures essential aspects of complex sounds in the natural environment. Previously, we showed that under controlled laboratory conditions, young listeners sampled from the university subject pool (n = 10) performed very well in detecting targets embedded in the stochastic figure-ground signal. Here, we presented a modified version of this cocktail party paradigm as a ‘game’ featured in a smartphone app (The Great Brain Experiment) and obtained data from a large population with diverse demographical patterns (n = 5148). Despite differences in paradigms and experimental settings, the observed target-detection performance by users of the app was robust and consistent with our previous results from the psychophysical study. Our results highlight the potential use of smartphone apps in capturing robust large-scale auditory behavioral data from normal healthy volunteers, which can also be extended to study auditory deficits in clinical populations with hearing impairments and central auditory disorders.     

Experience Matters: Females Use Smell to Select Experienced Males for Paternal Care

Mate choice and mating preferences often rely on the information content of signals exchanged between potential partners. In species where a female''s reproduction is the terminal event in life it is to be expected that females choose high quality males and assess males using some honest indicator of male quality. The Nereidid polychaete, Neanthes acuminata, exhibits monogamous pairing and the release of eggs by females terminates her life and larval success relies entirely on a male''s ability to provide paternal care. As such females should have developed reliable, condition-dependent criteria to choose mates to guarantee survival and care for offspring. We show that females actively chose males experienced in fatherhood over others. In the absence of experienced males dominance, as evident from male-male fights, is utilized for mate selection. The preference for experienced males is not affected by previous social interactions between the individuals. We show that the choice of the partner is based on chemical signals demonstrating a ‘scent of experience’ to females providing evidence for the role of chemical signals in sexual selection for paternal care adding to our understanding of the mechanisms regulating condition-dependent mate choice.     

Baby on board: olfactory cues indicate pregnancy and fetal sex in a non-human primate

Olfactory cues play an integral, albeit underappreciated, role in mediating vertebrate social and reproductive behaviour. These cues fluctuate with the signaller''s hormonal condition, coincident with and informative about relevant aspects of its reproductive state, such as pubertal onset, change in season and, in females, timing of ovulation. Although pregnancy dramatically alters a female''s endocrine profiles, which can be further influenced by fetal sex, the relationship between gestation and olfactory cues is poorly understood. We therefore examined the effects of pregnancy and fetal sex on volatile genital secretions in the ring-tailed lemur (Lemur catta), a strepsirrhine primate possessing complex olfactory mechanisms of reproductive signalling. While pregnant, dams altered and dampened their expression of volatile chemicals, with compound richness being particularly reduced in dams bearing sons. These changes were comparable in magnitude with other, published chemical differences among lemurs that are salient to conspecifics. Such olfactory ‘signatures’ of pregnancy may help guide social interactions, potentially promoting mother–infant recognition, reducing intragroup conflict or counteracting behavioural mechanisms of paternity confusion; cues that also advertise fetal sex may additionally facilitate differential sex allocation.     

Cry-wolf signals emerging from coevolutionary feedbacks in a tritrophic system

For a communication system to be stable, senders should convey honest information. Providing dishonest information, however, can be advantageous to senders, which imposes a constraint on the evolution of communication systems. Beyond single populations and bitrophic systems, one may ask whether stable communication systems can evolve in multitrophic systems. Consider cross-species signalling where herbivore-induced plant volatiles (HIPVs) attract predators to reduce the damage from arthropod herbivores. Such plant signals may be honest and help predators to identify profitable prey/plant types via HIPV composition and to assess prey density via the amount of HIPVs. There could be selection for dishonest signals that attract predators for protection from possible future herbivory. Recently, we described a case in which plants release a fixed, high amount of HIPVs independent of herbivore load, adopting what we labelled a ‘cry-wolf’ strategy. To understand when such signals evolve, we model coevolutionary interactions between plants, herbivores and predators, and show that both ‘honest’ and ‘cry-wolf’ types can emerge, depending on the assumed plant–herbivore encounter rates and herbivore population density. It is suggested that the ‘cry-wolf’ strategy may have evolved to reduce the risk of heavy damage in the future. Our model suggests that eco-evolutionary feedback loops involving a third species may have important consequences for the stability of this outcome.