Forewarned is forearmed: Queensland fruit flies detect olfactory cues from predators and respond with predator-specific behaviour.
ABSTRACT: Animals can gain significant advantages from abilities to detect cues from predators, assess risks, and respond adaptively to reduce the likelihood of injurious interactions. In contrast, predator cue-induced changes in behaviour may interfere with fitness-associated activities such as exploration, foraging and reproduction. Despite the ecological importance of predator-prey interactions in insects, remarkably little is known about the abilities of insects to detect and respond to olfactory cues from predators, or the potential costs of such responses. We here demonstrate that a tephritid fruit fly, the Queensland fruit fly Bactrocera tryoni, is able to detect and respond differentially to volatile olfactory cues from four potential predators (three spiders and an ant) that vary in prevalence and diurnal activity. Male and female flies increased or decreased motility (velocity, active time, distance moved), or exhibited no change in motility, depending on which predator volatiles they encountered. Further, flies significantly reduced foraging, oviposition and mating propensity in the presence of volatiles from any of the predators. This study is the first report of predator-specific responses to olfactory cues in a tephritid fruit fly, and highlights that such anti-predator responses can impose costs on general activity and reproductive behaviour.
Project description:Chemical cues play important roles in predator-prey interactions. Semiochemicals can aid predator foraging and alert prey organisms to the presence of predators. Previous work suggests that predator traits differentially influence prey behavior, however, empirical data on how prey organisms respond to chemical cues from predator species with different hunting strategies, and how foraging predators react to cues from potential competitors, is lacking. Furthermore, most research in this area has focused on aquatic and aboveground terrestrial systems, while interactions among belowground, soiling-dwelling organisms have received relatively little attention. Here, we assessed how chemical cues from three species of entomopathogenic nematodes (EPNs), each with a different foraging strategy, influenced herbivore (cucumber beetle) and natural enemy (EPN) foraging behavior. We predicted these cues could serve as chemical indicators of increased predation risk, prey availability, or competition. Our findings revealed that foraging cucumber beetle larvae avoided chemical cues from Heterorhabditis bacteriophora (active-foraging cruiser EPNs), but not Steinernema carpocapsae (ambusher EPNs) or Steinernema riobrave (intermediate-foraging EPNs). In contrast, foraging H. bacteriophora EPNs were attracted to cues produced by the two Steinernema species but not conspecific cues. Notably, the three EPN species produced distinct blends of olfactory cues, with only a few semi-conserved compounds across species. These results indicate that a belowground insect herbivore responds differently to chemical cues from different EPN species, with some EPN species avoiding prey detection. Moreover, the active-hunting EPNs were attracted to heterospecific cues, suggesting these cues indicate a greater probability of available prey, rather than strong interspecific competition.
Project description:Most animals are faced with the challenge of securing food under the risk of predation. This frequently generates a trade-off whereby animals respond to predator cues with reduced movement to avoid predation at the direct cost of reduced foraging success. However, predators may also cause prey to be apprehensive in their foraging activities, which would generate an indirect 'apprehension cost'. Apprehension arises when a forager redirects attention from foraging tasks to predator detection and incurs a cost from such multi-tasking, because the forager ends up making more mistakes in its foraging tasks as a result. Here, we test this apprehension cost hypothesis and show that damselflies miss a greater proportion of their prey during foraging bouts in response to both olfactory cues produced by conspecifics that have only viewed a fish predator and olfactory cues produced directly by fish. This reduced feeding efficiency is in addition to the stereotypical anti-predator response of reduced activity, which we also observed. These results show that costs associated with anti-predator responses not only arise through behavioural alterations that reduce the risk of predation, but also from the indirect costs of apprehension and multi-tasking that can reduce feeding efficiency under the threat of predation.
Project description:AbstractPrey strategically respond to the risk of predation by varying their behavior while balancing the tradeoffs of food and safety. We present here an experiment that tests the way the same indirect cues of predation risk are interpreted by bank voles, Myodes glareolus, as the game changes through exposure to a caged weasel. Using optimal patch use, we asked wild-caught voles to rank the risk they perceived. We measured their response to olfactory cues in the form of weasel bedding, a sham control in the form of rabbit bedding, and an odor-free control. We repeated the interviews in a chronological order to test the change in response, i.e., the changes in the value of the information. We found that the voles did not differentiate strongly between treatments pre-exposure to the weasel. During the exposure, vole foraging activity was reduced in all treatments, but proportionally increased in the vicinity to the rabbit odor. Post-exposure, the voles focused their foraging in the control, while the value of exposure to the predator explained the majority of variation in response. Our data also suggested a sex bias in interpretation of the cues. Given how the foragers changed their interpretation of the same cues based on external information, we suggest that applying predator olfactory cues as a simulation of predation risk needs further testing. For instance, what are the possible effective compounds and how they change “fear” response over time. The major conclusion is that however effective olfactory cues may be, the presence of live predators overwhelmingly affects the information voles gained from these cues.Significance statementIn ecology, “fear” is the strategic response to cues of risk an animal senses in its environment. The cues suggesting the existence of a predator in the vicinity are weighed by an individual against the probability of encounter with the predator and the perceived lethality of an encounter with the predator. The best documented such response is variation in foraging tenacity as measured by a giving-up density. In this paper, we show that an olfactory predator cue and the smell of an interspecific competitor result in different responses based on experience with a live-caged predator. This work provides a cautionary example of the risk in making assumptions regarding olfactory cues devoid of environmental context.Electronic supplementary materialThe online version of this article (10.1007/s00265-018-2600-9) contains supplementary material, which is available to authorized users.
Project description:Coral reefs around the world are rapidly degrading due to a range of environmental stressors. Habitat degradation modifies the sensory landscape within which predator-prey interactions occur, with implications for olfactory-mediated behaviours. Predator naïve settlement-stage damselfish rely on conspecific damage-released odours (i.e., alarm odours) to inform risk assessments. Yet, species such as the Ambon damselfish, Pomacentrus amboinensis, become unable to respond appropriately to these cues when living in dead-degraded coral habitats, leading to increased mortality through loss of vigilance. Reef fish predators also rely on odours from damaged prey to locate, assess prey quality and engage in prey-stealing, but it is unknown whether their responses are also modified by the change to dead-degraded coral habitats. Implications for prey clearly depend on how their predatory counterparts are affected, therefore the present study tested whether olfactory-mediated foraging responses in the dusky dottyback, Pseudochromis fuscus, a common predator of P. amboinensis, were similarly affected by coral degradation. A y-maze was used to measure the ability of Ps. fuscus to detect and move towards odours, against different background water sources. Ps. fuscus were exposed to damage-released odours from juvenile P. amboinensis, or a control cue of seawater, against a background of seawater treated with either healthy or dead-degraded hard coral. Predators exhibited an increased time allocation to the chambers of y-mazes injected with damage-released odours, with comparable levels of response in both healthy and dead-degraded coral treated waters. In control treatments, where damage-released odours were replaced with a control seawater cue, fish showed no increased preference for either chamber of the y-maze. Our results suggest that olfactory-mediated foraging behaviours may persist in Ps. fuscus within dead-degraded coral habitats. Ps. fuscus may consequently gain a sensory advantage over P. amboinensis, potentially altering the outcome of predator-prey interactions.
Project description:For animals to survive until reproduction, it is crucial that juveniles successfully detect potential predators and respond with appropriate behavior. The recognition of cues originating from predators can be innate or learned. Cues of various modalities might be used alone or in multi-modal combinations to detect and distinguish predators but studies investigating multi-modal integration in predator avoidance are scarce. Here, we used wild, naive tadpoles of the Neotropical poison frog Allobates femoralis ( Boulenger, 1884) to test their reaction to cues with two modalities from two different sympatrically occurring potential predators: heterospecific predatory Dendrobates tinctorius tadpoles and dragonfly larvae. We presented A. femoralis tadpoles with olfactory or visual cues, or a combination of the two, and compared their reaction to a water control in a between-individual design. In our trials, A. femoralis tadpoles reacted to multi-modal stimuli (a combination of visual and chemical information) originating from dragonfly larvae with avoidance but showed no reaction to uni-modal cues or cues from heterospecific tadpoles. In addition, visual cues from conspecifics increased swimming activity while cues from predators had no effect on tadpole activity. Our results show that A. femoralis tadpoles can innately recognize some predators and probably need both visual and chemical information to effectively avoid them. This is the first study looking at anti-predator behavior in poison frog tadpoles. We discuss how parental care might influence the expression of predator avoidance responses in tadpoles.
Project description:Exposure to olfactory cues during embryonic development can have long term impacts on birds and amphibians behaviour. Despite the vast literature on predator recognition and responses in fishes, few researchers have determined how fish embryos respond to predator cues. Here we exposed four-day-old rainbowfish (Melanotaenia duboulayi) embryos to cues emanating from a novel predator, a native predator and injured conspecifics. Their response was assessed by monitoring heart rate and hatch time. Results showed that embryos have an innate capacity to differentiate between cues as illustrated by faster heart rates relative to controls. The greatest increase in heart rate occurred in response to native predator odour. While we found no significant change in the time taken for eggs to hatch, all treatments experienced slight delays as expected if embryos are attempting to reduce exposure to larval predators.
Project description:Summary Chemical signals mediate major ecological interactions in insects. However, using bioassays only, it is difficult to quantify the bioactivity of complex mixtures, such as volatile defensive secretions emitted by prey insects, and to assess the impact of single compounds on the repellence of the entire mixture. To represent chemical data in a different perceptive mode, we used a process of sonification by parameter mapping of single molecules, which translated chemical signals into acoustic signals. These sounds were then mixed at dB levels reflecting the relative concentrations of the molecules within species-specific secretions. Repellence of single volatiles, as well as mixtures of volatiles, against predators were significantly correlated with the repulsiveness of their respective auditory translates against humans, who mainly reacted to sound pressure. Furthermore, sound pressure and predator response were associated with the number of different molecules in a secretion. Our transmodal approach, from olfactory to auditory perception, offers further prospects for chemo-ecological research and data representation. Highlights • The defensive secretion emitted by insects is often a mixture of volatiles• Volatiles were translated into sounds by sonification using parameter mapping• Chemical signals were repulsive for predators, as were the sounds for humans The bigger picture Insects are often defended against predators by emitting volatile secretions that act as a repellent. Chemical analyses of a secretion provide a list of compounds and their concentrations, but it then remains challenging to study their single and combined bioactivities. Here, we provide a first approach in understanding the bioactivity of single volatiles and volatile mixtures by developing a process of sonification (parameter mapping) to model chemical signals into auditory ones. Our study reveals via bioassays that foraging predators are repelled by volatiles as are human volunteers upon hearing "sonified volatiles". In these audio clips, we could also identify one sound attribute, their maximal loudness, that correlates well with the human response in the modeled world and hence with the predator response in the real world. These findings may help in exploring and understanding the seemingly overabundant diversity of deleterious chemicals present in insects and other organisms. A methodology is described to predict and compare the interspecific repellence of defensive secretions from insects that typically emit volatiles as complex mixtures. Sonification by parameter mapping allowed us to hear single molecules, then their mixtures. Bioassays used insect predators tested against the two sets of stimuli, single and mixed volatiles, as well as humans hearing the corresponding auditory translates. The model based on gathered chemical data can serve as a proxy but quantitative indicator of repellent bioactivities.
Project description:Animals such as bumblebees use chemosensory cues to both locate and evaluate essential resources. Increasingly, it is recognized that microbes can alter the quality of foraged resources and produce metabolites that may act as foraging cues. The distinct nature of these chemosensory cues however and their use in animal foraging remain poorly understood. Here, we test the hypothesis that species of nectar-inhabiting microbes differentially influence pollinator attraction and feeding via microbial metabolites produced in nectar. We first examined the electrophysiological potential for bumblebee (Bombus impatiens) antennal olfactory neurons to respond to microbial volatile organic compounds (mVOCs), followed by an olfactory preference test. We also assessed gustatory preferences for microbial-altered nectar through both no-choice and choice feeding assays. Antennal olfactory neurons responded to some mVOCs, and bees preferred nectar solutions inoculated with the bacterium Asaia astilbes over the yeast Metschnikowia reukaufii based on volatiles alone. However, B. impatiens foragers consumed significantly more Metschnikowia-inoculated nectar, suggesting distinct roles for mVOCs and non-volatile metabolites in mediating both attraction and feeding decisions. Collectively, our results suggest that microbial metabolites have significant potential to shape interspecific, plant-pollinator signalling, with consequences for forager learning, economics and floral host reproduction.
Project description:Novel stimuli elicit behaviors that are collectively known as specific exploration. These behaviors allow the animal to become more familiar with the novel objects within its environment. Specific exploration is frequently suppressed by defensive reactions to predator cues. Herein, we examine if this suppression occurs in Drosophila melanogaster by measuring the response of these flies to wild harvested predators. The flies used in our experiments have been cultured and had not lived under predator threat for multiple decades. In a circular arena with centrally-caged predators, wild type Drosophila actively avoided the pantropical jumping spider, Plexippus paykulli, and the Texas unicorn mantis, Phyllovates chlorophaena, indicating an innate defensive reaction to these predators. Interestingly, wild type Drosophila males also avoided a centrally-caged mock spider, and the avoidance of the mock spider became exaggerated when it was made to move within the cage. Visually impaired Drosophila failed to detect and avoid the Plexippus paykulli and the moving mock spider, while the broadly anosmic orco2 mutants were fully capable of detecting and avoiding Plexippus paykulli, indicating that these flies principally relied upon vison to perceive the predator stimuli. During early exploration of the arena, exploratory activity increased in the presence of Plexippus paykulli and the moving mock spider. The elevated activity induced by Plexippus paykulli disappeared after the fly had finished exploring, suggesting the flies were capable of habituating the predator cues. Taken together, these results indicate that despite being isolated from predators for decades Drosophila will visually detect these predators, retain innate defensive behaviors, respond by increasing exploratory activity in the arena rather than suppressing activity, and may habituate to normal predator cues.
Project description:Exposure to plant compounds and analogues of juvenile hormone (JH) increase male mating success in several species of tephritid fruit flies. Most of these species exhibit a lek mating system, characterized by active female choice. Although the pattern of enhanced male mating success is evident, few studies have investigated what benefits, if any, females gain via choice of exposed males in the lek mating system. In the South American fruit fly, Anastrepha fraterculus, females mate preferentially with males that were exposed to volatiles released by guava fruit or treated with methoprene (a JH analogue). Here, we tested the hypothesis that female choice confers direct fitness benefits in terms of fecundity and fertility. We first carried out mate choice experiments presenting females with males treated and non-treated with guava volatiles or, alternatively, treated and non-treated with methoprene. After we confirmed female preference for treated males, we compared the fecundity and fertility between females mated with treated males and non-treated ones. We found that A. fraterculus females that mated with males exposed to guava volatiles showed higher fecundity than females mated to non-exposed males. On the other hand, females that mated methoprene-treated males showed no evidence of direct benefits. Our findings represent the first evidence of a direct benefit associated to female preference for males that were exposed to host fruit odors in tephritid fruit flies. Differences between the two treatments are discussed in evolutionary and pest management terms.