Organisms face the cognitive challenge of making decisions based on imperfect information. Predators and prey, in particular, are confronted with ambiguous stimuli when foraging and avoiding attacks. ...These challenges are accentuated by variation imposed by environmental, physiological, and cognitive factors. While the cognitive factors influencing perceived ambiguity are often assumed to be fixed, contemporary findings reveal that perceived ambiguity is instead the dynamic outcome of interactive cognitive processes. Here, we present a framework that integrates recent advances in neurophysiology and sensory ecology with a classic decision-making model, signal detection theory (SDT), to understand the cognitive mechanisms that shape perceived stimulus ambiguity in predators and prey. Since stimulus ambiguity is pervasive, the framework discussed here provides insights that extend into nonforaging contexts.
Advances in neurophysiology and sensory ecology are unraveling the mechanisms that shape an organism’s perception of ambiguous stimuli.Sensory filters, neural noise, iterative sampling, attention, and integration of multiple stimulus components and modalities, and their interactions with state-dependent effects, collectively modify perceived stimulus ambiguity.Decisions made by predators (foraging) and prey (defense and escape) provide fertile ground to integrate recent advancements on the neural mechanism underlying decision-making.Placing these advances in an ecological context reveals that modifiers of stimulus ambiguity, both internal and external to an organism, interact dynamically to affect decision-making and can potentially alter ecological and evolutionary processes.
To thoroughly understand the drivers of dynamic signal elaboration requires assessing the direct and indirect effects of naturally interacting factors. Here, we use structural equation modeling to ...test multivariate data from in situ observations of sexual signal production against a model of causal processes hypothesized to drive signal elaboration. We assess direct and indirect effects, and relative impacts, of male-male competition and attacks by eavesdropping frog-biting midges (Diptera: Corethrellidae) on call elaboration of male túngara frogs (Engystomops pustulosus). We find that the intensity of attacks by these micropredator flies drives the extent to which frogs elaborate their calls, likely due to a temporal trade-off between signaling and antimicropredator defense. Micropredator attacks appear to dynamically limit a male’s call rate and complexity and consequently dampen the effects of intrasexual competition. In accounting for naturally interacting drivers of signal elaboration, this study presents a counterpoint to the mechanisms traditionally thought to drive sexual selection in this system. Moreover, the results shed light on the relatively unexamined and potentially influential role of eavesdropping micropredators in the evolution of sexual communication systems.
Significance Bats and moths have been engaged in acoustic warfare for more than 60 million y. Yet almost half of moth species lack bat-detecting ears and still face intense bat predation. We ...hypothesized that the long tails of one group of seemingly defenseless moths, saturniids, are an anti-bat strategy designed to divert bat attacks. Using high-speed infrared videography, we show that the spinning hindwing tails of luna moths lure echolocating bat attacks to these nonessential appendages in over half of bat–moth interactions. Further we show that long hindwing tails have independently evolved multiple times in saturniid moths. This finding expands our knowledge of antipredator deflection strategies, the limitations of bat sonar, and the extent of a long-standing evolutionary arms race.
Adaptations to divert the attacks of visually guided predators have evolved repeatedly in animals. Using high-speed infrared videography, we show that luna moths ( Actias luna ) generate an acoustic diversion with spinning hindwing tails to deflect echolocating bat attacks away from their body and toward these nonessential appendages. We pit luna moths against big brown bats ( Eptesicus fuscus ) and demonstrate a survival advantage of ∼47% for moths with tails versus those that had their tails removed. The benefit of hindwing tails is equivalent to the advantage conferred to moths by bat-detecting ears. Moth tails lured bat attacks to these wing regions during 55% of interactions between bats and intact luna moths. We analyzed flight kinematics of moths with and without hindwing tails and suggest that tails have a minimal role in flight performance. Using a robust phylogeny, we find that long spatulate tails have independently evolved four times in saturniid moths, further supporting the selective advantage of this anti-bat strategy. Diversionary tactics are perhaps more common than appreciated in predator–prey interactions. Our finding suggests that focusing on the sensory ecologies of key predators will reveal such countermeasures in prey.
Emitting conspicuous signals into the environment to attract mates comes with the increased risk of interception by eavesdropping enemies. As a defence, a commonly described strategy is for ...signallers to group together in leks, diluting each individual's risk. Lekking systems are often highly social settings in which competing males dynamically alter their signalling behaviour to attract mates. Thus, signalling at the lek requires navigating fluctuations in risk, competition and reproductive opportunities. Here, we investigate how behavioural defence strategies directed at an eavesdropping enemy have cascading effects across the communication network. We investigated these behaviours in the túngara frog (
), examining how a calling male's swatting defence directed at frog-biting midges indirectly affects the calling behaviour of his rival. We found that the rival responds to swat-induced water ripples by increasing his call rate and complexity. Then, performing phonotaxis experiments, we found that eavesdropping fringe-lipped bats (
) do not exhibit a preference for a swatting male compared to his rival, but females strongly prefer the rival male. Defences to minimize attacks from eavesdroppers thus shift the mate competition landscape in favour of rival males. By modulating the attractiveness of signalling prey to female receivers, we posit that eavesdropping micropredators likely have an unappreciated impact on the ecology and evolution of sexual communication systems.
Warning signals are well known in the visual system, but rare in other modalities. Some moths produce ultrasonic sounds to warn bats of noxious taste or to mimic unpalatable models. Here, we report ...results from a long-term study across the globe, assaying moth response to playback of bat echolocation. We tested 252 genera, spanning most families of large-bodied moths, and document anti-bat ultrasound production in 52 genera, with eight subfamily origins described. Based on acoustic analysis of ultrasonic emissions and palatability experiments with bats, it seems that acoustic warning and mimicry are the raison d'être for sound production in most moths. However, some moths use high-duty-cycle ultrasound capable of jamming bat sonar. In fact, we find preliminary evidence of independent origins of sonar jamming in at least six subfamilies. Palatability data indicate that jamming and warning are not mutually exclusive strategies. To explore the possible organization of anti-bat warning sounds into acoustic mimicry rings, we intensively studied a community of moths in Ecuador and, using machine-learning approaches, found five distinct acoustic clusters. While these data represent an early understanding of acoustic aposematism and mimicry across this megadiverse insect order, it is likely that ultrasonically signaling moths comprise one of the largest mimicry complexes on earth.
A synthesis of deimatic behaviour Drinkwater, Eleanor; Allen, William L.; Endler, John A. ...
Biological reviews of the Cambridge Philosophical Society,
December 2022, 2022-12-00, 20221201, Letnik:
97, Številka:
6
Journal Article
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ABSTRACT
Deimatic behaviours, also referred to as startle behaviours, are used against predators and rivals. Although many are spectacular, their proximate and ultimate causes remain unclear. In this ...review we aim to synthesise what is known about deimatic behaviour and identify knowledge gaps. We propose a working hypothesis for deimatic behaviour, and discuss the available evidence for the evolution, ontogeny, causation, and survival value of deimatic behaviour using Tinbergen's Four Questions as a framework. Our overarching aim is to direct future research by suggesting ways to address the most pressing questions in this field.
Most mosquito and midge species use hearing during acoustic mating behaviors. For frog-biting species, however, hearing plays an important role beyond mating as females rely on anuran calls to obtain ...blood meals. Despite the extensive work examining hearing in mosquito species that use sound in mating contexts, our understanding of how mosquitoes hear frog calls is limited. Here, we directly investigated the mechanisms underlying detection of frog calls by a mosquito species specialized on eavesdropping on anuran mating signals: Uranotaenia lowii. Behavioral, biomechanical and neurophysiological analyses revealed that the antenna of this frog-biting species can detect frog calls by relying on neural and mechanical responses comparable to those of non-frog-biting species. Our findings show that in Ur. lowii, contrary to most species, males do not use sound for mating, but females use hearing to locate their anuran host. We also show that the response of the antennae of this frog-biting species resembles that of the antenna of species that use hearing for mating. Finally, we discuss our data considering how mosquitoes may have evolved the ability to tap into the communication system of frogs.
The evolution and ecology of multiple antipredator defences Kikuchi, David W.; Allen, William L.; Arbuckle, Kevin ...
Journal of evolutionary biology,
July 2023, 2023-07-00, 2023-07-01, 20230701, 2023-07, Letnik:
36, Številka:
7
Journal Article
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Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple ...defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade‐offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.
Evolution of multiple defences as a function of trade‐offs & synergies among traits, ecology & evolutionary history, genetics & development, predator cognition.
Many defended animals prevent attacks by displaying warning signals that are highly conspicuous to their predators. We hypothesized that bioluminescing fireflies, widely known for their vibrant ...courtship signals, also advertise their noxiousness to echolocating bats. To test this postulate, we pit naïve big brown bats (
) against chemically defended fireflies (
) to examine whether and how these beetles transmit salient warnings to bats. We demonstrate that these nocturnal predators learn to avoid noxious fireflies using either vision or echolocation and that bats learn faster when integrating information from both sensory streams-providing fundamental evidence that multisensory integration increases the efficacy of warning signals in a natural predator-prey system. Our findings add support for a warning signal origin of firefly bioluminescence and suggest that bat predation may have driven evolution of firefly bioluminescence.
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