Prey can detect predators via electroreception in air.

Predators and prey benefit from detecting sensory cues of each other's presence. As they move through their environment, terrestrial animals accumulate electrostatic charge. Because electric charges exert forces at a distance, a prey animal could conceivably sense electrical forces to detect an approaching predator. Here, we report such a case of a terrestrial animal detecting its predators by electroreception. We show that predatory wasps are charged, thus emit electric fields, and that caterpillars respond to such fields with defensive behaviors. Furthermore, the mechanosensory setae of caterpillars are deflected by these electrostatic forces and are tuned to the wingbeat frequency of their insect predators. This ability unveils a dimension of the sensory interactions between prey and predators and is likely widespread among terrestrial animals.

Parasite effects on receivers in animal communication: Hidden impacts on behavior, ecology, and evolution.

Parasites exert a profound effect on biological processes. In animal communication, parasite effects on signalers are well-known drivers of the evolution of communication systems. Receiver behavior is also likely to be altered when they are parasitized or at risk of parasitism, but these effects have received much less attention. Here, we present a broad framework for understanding the consequences of parasitism on receivers for behavioral, ecological, and evolutionary processes. First, we outline the different kinds of effects parasites can have on receivers, including effects on signal processing from the many parasites that inhabit, occlude, or damage the sensory periphery and the central nervous system or that affect physiological processes that support these organs, and effects on receiver response strategies. We then demonstrate how understanding parasite effects on receivers could answer important questions about the mechanistic causes and functional consequences of variation in animal communication systems. Variation in parasitism levels is a likely source of among-individual differences in response to signals, which can affect receiver fitness and, through effects on signaler fitness, impact population levels of signal variability. The prevalence of parasitic effects on specific sensory organs may be an important selective force for the evolution of elaborate and multimodal signals. Finally, host-parasite coevolution across heterogeneous landscapes will generate geographic variation in communication systems, which could ultimately lead to evolutionary divergence. We discuss applications of experimental techniques to manipulate parasitism levels and point the way forward by calling for integrative research collaborations between parasitologists, neurobiologists, and behavioral and evolutionary ecologists.

Repeated Divergence in Opsin Gene Expression Mirrors Photic Habitat Changes in Rapidly Evolving Crater Lake Cichlid Fishes.

AbstractSelection pressures differ along environmental gradients, and traits tightly linked to fitness (e.g., the visual system) are expected to track such variation. Along gradients, adaptation to local conditions might be due to heritable and nonheritable environmentally induced variation. Disentangling these sources of phenotypic variation requires studying closely related populations in nature and in the laboratory. The Nicaraguan lakes represent an environmental gradient in photic conditions from clear crater lakes to very turbid great lakes. From two old, turbid great lakes, Midas cichlid fish (Amphilophus cf. citrinellus) independently colonized seven isolated crater lakes of varying light conditions, resulting in a small adaptive radiation. We estimated variation in visual sensitivities along this photic gradient by measuring cone opsin gene expression among lake populations. Visual sensitivities observed in all seven derived crater lake populations shifted predictably in direction and magnitude, repeatedly mirroring changes in photic conditions. Comparing wild-caught and laboratory-reared fish revealed that 48% of this phenotypic variation is genetically determined and evolved rapidly. Decreasing intrapopulation variation as environments become spectrally narrower suggests that different selective landscapes operate along the gradient. We conclude that the power to predict phenotypic evolution along gradients depends on both the magnitude of environmental change and the selective landscape shape.

Morphology of nares associated with stereo-olfaction in baleen whales.

The sensory mechanisms used by baleen whales (Mysticeti) for locating ephemeral, dense prey patches in vast marine habitats are poorly understood. Baleen whales have a functional olfactory system with paired rather than single blowholes (nares), potentially enabling stereo-olfaction. Dimethyl sulfide (DMS) is an odorous gas emitted by phytoplankton in response to grazing by zooplankton. Some seabirds use DMS to locate prey, but this ability has not been demonstrated in whales. For 14 extant species of baleen whale, nares morphometrics (imagery from unoccupied aerial systems, UAS) was related to published trophic level indices using Bayesian phylogenetic mixed modelling. A significant negative relationship was found between nares width and whale trophic level (ß = -0.08, lower 95% CI = -0.13, upper 95% CI = -0.03), corresponding with a 39% increase in nares width from highest to lowest trophic level. Thus, species with nasal morphology best suited to stereo-olfaction are more zooplanktivorous. These findings provide evidence that some baleen whale species may be able to localize odorants e.g. DMS. Our results help direct future behavioural trials of olfaction in baleen whales, by highlighting the most appropriate species to study. This is a research priority, given the potential for DMS-mediated plastic ingestion by whales.

Smell throughout the life course.

The sense of smell is an important mediator of health and sociality at all stages of life, yet it has received limited attention in our lineage. Olfaction starts in utero and participates in the establishment of social bonds in children, and of romantic and sexual relationships after puberty. Smell further plays a key role in food assessment and danger avoidance; in modern societies, it also guides our consumer behavior. Sensory abilities typically decrease with age and can be impacted by diseases, with repercussions on health and well-being. Here, we critically review our current understanding of human olfactory communication to refute outdated notions that our sense of smell is of low importance. We provide a summary of the biology of olfaction, give a prospective overview of the importance of the sense of smell throughout the life course, and conclude with an outline of the limitations and future directions in this field.

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.

Seed dispersal syndrome predicts ethanol concentration of fruits in a tropical dry forest.

Studying fruit traits and their interactions with seed dispersers can improve how we interpret patterns of biodiversity, ecosystem function and evolution. Mounting evidence suggests that fruit ethanol is common and variable, and may exert selective pressures on seed dispersers. To test this, we comprehensively assess fruit ethanol content in a wild ecosystem and explore sources of variation. We hypothesize that both phylogeny and seed dispersal syndrome explain variation in ethanol levels, and we predict that fruits with mammalian dispersal traits will contain higher levels of ethanol than those with bird dispersal traits. We measured ripe fruit ethanol content in species with mammal- (n = 16), bird- (n = 14) or mixed-dispersal (n = 7) syndromes in a Costa Rican tropical dry forest. Seventy-eight per cent of fruit species yielded measurable ethanol concentrations. We detected a phylogenetic signal in maximum ethanol levels (Pagel's λ = 0.82). Controlling for phylogeny, we observed greater ethanol concentrations in mammal-dispersed fruits, indicating that dispersal syndrome helps explain variation in ethanol content, and that mammals may be more exposed to ethanol in their diets than birds. Our findings further our understanding of wild fruit ethanol and its potential role as a selective pressure on frugivore sensory systems and metabolism.

Experimental test of the influence of light availability on the evolution of eye size and behaviour in Daphnia.

There exists extensive variation in eye size. Much work has provided a connection between light availability and differences in eye size across taxa. Experimental tests of the role of the light environment on the evolution of eye size are lacking. Here, we performed a selection experiment that examined the influence of light availability on shifts in eye size and the connection between eye size and phototactic (anti-predator) behaviour in Daphnia. We set-up replicate experimental populations of Daphnia, repeatedly evaluated phenotypic shifts in eye size during the ~50-day experiment, and performed a common garden experiment at the end of the experiment to test for evolutionary shifts in eye size and behaviour. Our phenotypic analyses showed that eye size rapidly diverged between the light treatments; relative eye size was consistently larger in the low versus high light treatments. Selection on eye size was also modified by variation in density as increases in Daphnia density favoured a larger eye. However, we did not observe differences in eye size between the light treatments following two generations of common garden rearing at the end of the experiment. We instead observed strong shifts in anti-predator behaviour. Daphnia from the low light treatment exhibited decreased phototactic responses to light. Our results show that decreased light relaxes selection on anti-predator behaviour. Such trends provide new insights into selection on eye size and behaviour.

Visual environment of rearing sites affects larval response to perceived risk in poison frogs.

Turbidity challenges the visual performance of aquatic animals. Here, we use the natural diversity of ephemeral rearing sites occupied by tadpoles of two poison frog species to explore the relationship between environments with limited visibility and individual response to perceived risk. To compare how species with diverse natural histories respond to risk after developing in a range of photic environments, we sampled wild tadpoles of (1) Dendrobates tinctorius, a rearing-site generalist with facultatively cannibalistic tadpoles and (2) Oophaga pumilio, a small-pool specialist dependent on maternal food-provisioning. Using experimental arenas, we measured tadpole activity and space use first on a black and white background, and then on either black or white backgrounds where tadpoles were exposed to potentially predatory visual stimuli. The effects of rearing environment on D. tinctorius tadpoles were clear: tadpoles from darker pools were less active than tadpoles from brighter pools and did not respond to the visual stimuli, whereas tadpoles from brighter pools swam more when paired with conspecifics versus predatory insect larvae, suggesting that tadpoles can visually discriminate between predators. For O. pumilio, tadpoles were more active on experimental backgrounds that more closely matched the luminosity of their rearing sites, but their responses to the two visual stimuli did not differ. Larval specialisation associated with species-specific microhabitats may underlie the observed responses to visual stimuli. Our findings demonstrate that light availability in wild larval rearing conditions influences risk perception in novel contexts, and provides insight into how visually guided animals may respond to sudden environmental disturbances.

Passive electroreception in bottlenose dolphins (Tursiops truncatus): implication for micro- and large-scale orientation.

For the two dolphin species Sotalia guianensis (Guiana dolphin) and Tursiops truncatus (bottlenose dolphin), previous research has shown that the vibrissal crypts located on the rostrum represent highly innervated, ampullary electroreceptors and that both species are correspondingly sensitive to weak electric fields. In the present study, for a comparative assessment of the sensitivity of the bottlenose dolphin's electroreceptive system, we determined detection thresholds for DC and AC electric fields with two bottlenose dolphins. In a psychophysical experiment, the animals were trained to respond to electric field stimuli using the go/no-go paradigm. We show that the two bottlenose dolphins are able to detect DC electric fields as low as 2.4 and 5.5 µV cm-1, respectively, a detection threshold in the same order of magnitude as those in the platypus and the Guiana dolphin. Detection thresholds for AC fields (1, 5 and 25 Hz) were generally higher than those for DC fields, and the sensitivity for AC fields decreased with increasing frequency. Although the electroreceptive sensitivity of dolphins is lower than that of elasmobranchs, it is suggested that it allows for both micro- and macro-scale orientation. In dolphins pursuing benthic foraging strategies, electroreception may facilitate short-range prey detection and target-oriented snapping of their prey. Furthermore, the ability to detect weak electric fields may enable dolphins to perceive the Earth's magnetic field through induction-based magnetoreception, thus allowing large-scale orientation.

The evolution of prey-attraction strategies in spiders: the interplay between foraging and predator avoidance.

Lures and other adaptations for prey attraction are particularly interesting from an evolutionary viewpoint because they are characterized by correlational selection, involve multicomponent signals, and likely reflect a compromise between maximizing conspicuousness to prey while avoiding drawing attention of enemies and predators. Therefore, investigating the evolution of lure and prey-attraction adaptations can help us understand a larger set of traits governing interactions among organisms. We review the literature focusing on spiders (Araneae), which is the most diverse animal group using prey attraction and show that the evolution of prey-attraction strategies must be driven by a trade-off between foraging and predator avoidance. This is because increasing detectability by potential prey often also results in increased detectability by predators higher in the food chain. Thus increasing prey attraction must come at a cost of increased risk of predation. Given this trade-off, we should expect lures and other prey-attraction traits to remain suboptimal despite a potential to reach an optimal level of attractiveness. We argue that the presence of this trade-off and the multivariate nature of prey-attraction traits are two important mechanisms that might maintain the diversity of prey-attraction strategies within and between species. Overall, we aim to stimulate research on this topic and progress in our general understanding of the diversity of predator and prey interactions.

Wild hummingbirds discriminate nonspectral colors.

Many animals have the potential to discriminate nonspectral colors. For humans, purple is the clearest example of a nonspectral color. It is perceived when two color cone types in the retina (blue and red) with nonadjacent spectral sensitivity curves are predominantly stimulated. Purple is considered nonspectral because no monochromatic light (such as from a rainbow) can evoke this simultaneous stimulation. Except in primates and bees, few behavioral experiments have directly examined nonspectral color discrimination, and little is known about nonspectral color perception in animals with more than three types of color photoreceptors. Birds have four color cone types (compared to three in humans) and might perceive additional nonspectral colors such as UV+red and UV+green. Can birds discriminate nonspectral colors, and are these colors behaviorally and ecologically relevant? Here, using comprehensive behavioral experiments, we show that wild hummingbirds can discriminate a variety of nonspectral colors. We also show that hummingbirds, relative to humans, likely perceive a greater proportion of natural colors as nonspectral. Our analysis of plumage and plant spectra reveals many colors that would be perceived as nonspectral by birds but not by humans: Birds' extra cone type allows them not just to see UV light but also to discriminate additional nonspectral colors. Our results support the idea that birds can distinguish colors throughout tetrachromatic color space and indicate that nonspectral color perception is vital for signaling and foraging. Since tetrachromacy appears to have evolved early in vertebrates, this capacity for rich nonspectral color perception is likely widespread.

Great Gray Owls hunting voles under snow hover to defeat an acoustic mirage.

How do Great Gray Owls (Strix nebulosa) capture voles (Cricetidae) through a layer of snow? As snow is a visual barrier, the owls locate voles by ear alone. To test how snow absorbs and refracts vole sound, we inserted a loudspeaker under the snowpack and analysed sound from the loudspeaker, first buried, then unburied. Snow attenuation coefficients rose with frequency (0.3 dB cm-1 at 500 Hz, 0.6 dB cm-1 at 3 kHz) such that low-frequency sound transmitted best. The Great Gray Owl has the largest facial disc of any owl, suggesting they are adapted to use this low-frequency sound. We used an acoustic camera to spatially localize sound source location, and show that snow also refracts prey sounds (refractive index: 1.16). To an owl not directly above the prey, this refraction creates an 'acoustic mirage': prey acoustic position is offset from its actual location. Their hunting strategy defeats this mirage because they hover directly over prey, which is the listening position with least refraction and least attenuation. Among all birds, the Great Gray Owl has the most extreme wing morphologies associated with quiet flight. These extreme wing traits may function to reduce the sounds of hovering, with implications for bioinspiration.

Underwater visibility constrains the foraging behaviour of a diving pelagic seabird.

Understanding the sensory ecology of species is vital if we are to predict how they will function in a changing environment. Visual cues are fundamentally important for many predators when detecting and capturing prey. However, many marine areas have become more turbid through processes influenced by climate change, potentially affecting the ability of marine predators to detect prey. We performed the first study that directly relates a pelagic seabird species's foraging behaviour to oceanic turbidity. We collected biologging data from 79 foraging trips and 5472 dives of a visually dependent, pursuit-diving seabird, the Manx shearwater (Puffinus puffinus). Foraging behaviour was modelled against environmental variables affecting underwater visibility, including water turbidity, cloud cover and solar angle. Shearwaters were more likely to initiate area-restricted search and foraging dives in clearer waters. Underwater visibility also strongly predicted dive rate and depth, suggesting that fine-scale prey capture was constrained by the detectability of prey underwater. Our novel use of dynamic descriptors of underwater visibility suggests that visual cues are vital for underwater foraging. Our data indicate that climate change could negatively impact seabird populations by making prey more difficult to detect, compounded by the widely reported effects of reduced prey populations.

Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates (Alouatta palliata, Ateles geoffroyi and Cebus imitator) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and trichromats, while all Alouatta are trichomats. We use anatomical proxies to examine smell, taste and manual touch, and opsin genotyping to assess colour vision. We find that the frugivorous spider monkeys (Ateles geoffroyi) sniff fruits most often, omnivorous capuchins (Cebus imitator), the species with the highest manual dexterity, use manual touch most often, and that main olfactory bulb volume is a better predictor of sniffing behaviour than nasal turbinate surface area. We also identify an interaction between colour vision phenotype and use of other senses. Controlling for species, dichromats sniff and bite fruits more often than trichromats, and trichromats use manual touch to evaluate cryptic fruits more often than dichromats. Our findings reveal new relationships among dietary specialization, anatomical variation and foraging behaviour, and promote understanding of sensory system evolution.

Comparative morphology and soft tissue histology of the remote-touch bill-tip organ in three ibis species of differing foraging ecology.

Ibises (order: Pelecaniformes, family: Threskiornithidae) are probe-foraging birds that use 'remote-touch' to locate prey items hidden in opaque substrates. This sensory capability allows them to locate their prey using high-frequency vibrations in the substrate in the absence of other sensory cues. Remote-touch is facilitated by a specialised bill-tip organ, comprising high densities of mechanoreceptors (Herbst corpuscles) embedded in numerous foramina in the beak bones. Each foramen and its associated Herbst corpuscles make up a sensory unit, called a 'sensory pit'. These sensory pits are densely clustered in the distal portion of the beak. Previous research has indicated that interspecific differences in the extent of sensory pitting in the beak bones correlate with aquatic habitat use of ibises, and have been suggested to reflect different levels of remote-touch sensitivity. Our study investigates the interspecific differences in the bone and soft tissue histology of the bill-tip organs of three species of southern African ibises from different habitats (mainly terrestrial to mainly aquatic). We analysed the external pitting pattern on the bones, as well as internal structure of the beak using micro-CT scans and soft tissue histological sections of each species' bill-tip organs. The beaks of all three species contain remote-touch bill-tip organs and are described here in detail. Clear interspecific differences are evident between the species' bill-tip organs, both in terms of bone morphology and soft tissue histology. Glossy Ibises, which forage exclusively in wetter substrates, have a greater extent of pitting but lower numbers of Herbst corpuscles in each pit, while species foraging in drier substrates (Hadeda and Sacred Ibises) have more robust beaks, fewer pits and higher densities of Herbst corpuscles. Our data, together with previously published histological descriptions of the bill-tip organs of other remote-touch foraging bird species, indicate that species foraging in drier habitats have more sensitive bill-tip organs (based on their anatomy). The vibrations produced by prey (e.g., burrowing invertebrates) travel poorly in dry substrates compared with wetter ones (i.e., dry soil vs. mud or water), and thus we hypothesise that a more sensitive bill-tip organ may be required to successfully locate prey in dry substrates. Furthermore, our results indicate that the differences in bill-tip organ anatomy between the species reflect complex trade-offs between morphological constraints of beak shape and remote-touch sensitivity requirements, both of which are likely related to each species' foraging behaviour and substrate usage. Our study suggests that structures in the bone of the bill-tip organ could provide valuable osteological correlates for the associated soft tissues, and consequently may provide information on the sensory ecology and habitat usage of the birds in the absence of soft tissues.

Becoming nose-blind-Climate change impacts on chemical communication.

Chemical communication via infochemicals plays a pivotal role in ecological interactions, allowing organisms to sense their environment, locate predators, food, habitats, or mates. A growing number of studies suggest that climate change-associated stressors can modify these chemically mediated interactions, causing info-disruption that scales up to the ecosystem level. However, our understanding of the underlying mechanisms is scarce. Evidenced by a range of examples, we illustrate in this opinion piece that climate change affects different realms in similar patterns, from molecular to ecosystem-wide levels. We assess the importance of different stressors for terrestrial, freshwater, and marine ecosystems and propose a systematic approach to address highlighted knowledge gaps and cross-disciplinary research avenues.

Sea turtle hatchlings can distinguish between coastal and oceanic seawaters.

Following their emergence on land, sea turtle hatchlings need to travel through the open ocean. Whether hatchlings can detect ecologically and functionally relevant chemical cues released in the marine habitat is unknown. We collected seawater at 6 and 27 km off the Brazilian coast, i.e. within and beyond the continental shelf. In a two-choice flume, we exposed post-emergent (<24 h old) loggerhead (Caretta caretta) turtles to these seawaters. Based on their life history, we posited that if hatchlings could distinguish between the seawater from these regions, they should prefer the oceanic seawater and/or avoid the coastal seawater. Hatchlings were tested singly and could access any parts of the flume. We recorded the seawater plume first visited and the time spent in each plume. Of all the first choices and time spent in a plume, nearly 70% involved the oceanic seawater. The ability of hatchlings to distinguish between seawaters could provide goal-recognition information.

Nest sanitation as an effective defence against brood parasitism.

Egg rejection is a crucial defence strategy against brood parasitism that requires the host to correctly recognise the foreign egg. Rejection behaviour has, thus, evolved in many hosts, facilitated by the visual differences between the parasitic and host eggs, and driving hosts to rely on colour and pattern cues. On the other hand, the need to recognise non-egg-shaped objects to carry out nest sanitation led birds to evolve the ability to discriminate and eject objects using mainly shape cues. However, little is known regarding the evolutionary significance of rejection behaviour in general and the cognitive processes underlying it. Here, we investigated the response of the barn swallow (Hirundo rustica) during pre-laying and laying stages to four objects types that differed in shape (eggs vs stars) and colour/pattern (mimetic vs non-mimetic) to investigate (1) what cognitive mechanisms are involved in object discrimination and (2) whether egg rejection is a direct defence against brood parasitism, or simply a product of nest sanitation. We found that swallows ejected stars more often than eggs in both stages, indicating that swallows possess a template for the shape of their eggs. Since the effect of colour/pattern on ejection decisions was minor, we suggest that barn swallows have not evolved a direct defence against brood parasitism but instead, egg ejection might be a product of their well-developed nest sanitation behaviour. Nonetheless, the fact that mimetic eggs were ejected especially in the pre-laying stage shows that nest sanitation could be an effective defence against poorly timed brood parasitism.

Artificial light at night reverses monthly foraging pattern under simulated moonlight.

Mounting evidence shows that artificial light at night (ALAN) alters biological processes across levels of organization, from cells to communities. Yet, the combined impacts of ALAN and natural sources of night-time illumination remain little explored. This is in part due the lack of accurate simulations of the complex changes moonlight intensity, timing and spectra throughout a single night and lunar cycles in laboratory experiments. We custom-built a novel system to simulate natural patterns of moonlight to test how different ALAN intensities affect predator-prey relationships over the full lunar cycle. Exposure to high intensity ALAN (10 and 50 lx) reversed the natural lunar-guided foraging pattern by the gastropod mesopredator Nucella lapillus on its prey Semibalanus balanoides. Foraging decreased during brighter moonlight in naturally lit conditions. When exposed to high intensity ALAN, foraging increased with brighter moonlight. Low intensity ALAN (0.1 and 0.5 lx) had no impact on foraging. Our results show that ALAN alters the foraging pattern guided by changes in moonlight brightness. ALAN impacts on ecosystems can depend on lunar light cycles. Accurate simulations of night-time light cycle will warrant more realistic insights into ALAN impacts and also facilitate advances in fundamental night-time ecology and chronobiology.