Dazzle coloration and prey movement

Many traits in animals reduce the rate of attack from visually hunting predators, including camouflage, warning signals and mimicry. In addition, some animal markings may reduce the likelihood that an attack ends in successful capture. These might include dazzle markings, high-contrast patterns that make the estimation of speed and trajectory difficult. However, until now, no study has experimentally tested whether some markings may achieve such an effect. We developed a computer 'game' where human 'predators' have to capture computer-generated prey moving across a background. In two experiments, we find that although uniform camouflaged targets were among the hardest to capture, so were a range of high-contrast conspicuous patterns, such as bands and zigzags. Prey were also more difficult to capture against more heterogeneous than uniform backgrounds, and at faster speeds of movement. As such, we find the first experimental evidence that conspicuous patterns, similar to those found in a wide range of real animals, make the capture of moving prey more challenging. Various anti-predator markings may work prey during motion, and some animals may combine such dazzle patterns with other functions, such as camouflage, thermoregulation, sexual and warning signals.     

Artificial neural networks and the study of evolution of prey coloration

In this paper, I investigate the use of artificial neural networks in the study of prey coloration. I briefly review the anti-predator functions of prey coloration and describe both in general terms and with help of two studies as specific examples the use of neural network models in the research on prey coloration. The first example investigates the effect of visual complexity of background on evolution of camouflage. The second example deals with the evolutionary choice of defence strategy, crypsis or aposematism. I conclude that visual information processing by predators is central in evolution of prey coloration. Therefore, the capability to process patterns as well as to imitate aspects of predator's information processing and responses to visual information makes neural networks a well-suited modelling approach for the study of prey coloration. In addition, their suitability for evolutionary simulations is an advantage when complex or dynamic interactions are modelled. Since not all behaviours of neural network models are necessarily biologically relevant, it is important to validate a neural network model with empirical data. Bringing together knowledge about neural networks with knowledge about topics of prey coloration would provide a potential way to deepen our understanding of the specific appearances of prey coloration.     

Carnivorous pitcher plant uses free radicals in the digestion of prey

A study of the involvement of free oxygen radicals in trapping and digestion of insects by carnivorous plants was the main goal of the present investigation. We showed that the generation of oxygen free radicals by pitcher fluid of Nepenthes is the first step of the digestion process, as seen by EPR spin trapping assay and gel-electrophoresis. The EPR spectrum of N. gracilis fluid in the presence of DMPO spin trap showed the superposition of the hydroxyl radical spin adduct signal and of the ascorbyl radical signal. Catalase addition decreased the generation of hydroxyl radicals showing that hydroxyl radicals are generated from hydrogen peroxide, which can be derived from superoxide radicals. Gel-electrophoresis data showed that myosin, an abundant protein component of insects, can be rapidly broken down by free radicals and protease inhibitors do not inhibit this process. Addition of myoglobin to the pitcher plant fluid decreased the concentration of detectable radicals. Based on these observations, we conclude that oxygen free radicals produced by the pitcher plant aid in the digestion of the insect prey.     

Carnivorous pitcher plant uses free radicals in the digestion of prey

Abstract

A study of the involvement of free oxygen radicals in trapping and digestion of insects by carnivorous plants was the main goal of the present investigation. We showed that the generation of oxygen free radicals by pitcher fluid of Nepenthes is the first step of the digestion process, as seen by EPR spin trapping assay and gel-electrophoresis. The EPR spectrum of N. gracilis fluid in the presence of DMPO spin trap showed the superposition of the hydroxyl radical spin adduct signal and of the ascorbyl radical signal. Catalase addition decreased the generation of hydroxyl radicals showing that hydroxyl radicals are generated from hydrogen peroxide, which can be derived from superoxide radicals. Gel-electrophoresis data showed that myosin, an abundant protein component of insects, can be rapidly broken down by free radicals and protease inhibitors do not inhibit this process. Addition of myoglobin to the pitcher plant fluid decreased the concentration of detectable radicals. Based on these observations, we conclude that oxygen free radicals produced by the pitcher plant aid in the digestion of the insect prey.     

Correlated evolution between coloration and ambush site in predators with visual prey lures

The evolution of a visual signal will be affected by signaler and receiver behavior, and by the physical properties of the environment where the signal is displayed. Crab spiders are typical sit‐and‐wait predators found in diverse ambush sites, such as tree bark, foliage, and flowers. Some of the flower‐dweller species present a UV⁺‐white visual lure that makes them conspicuous and attractive to their prey. We hypothesized that UV⁺‐white coloration was associated with the evolution of a flower‐dwelling habit. In addition, following up on results from a previous study we tested whether the UV⁺‐white coloration evolved predominantly in flower‐dwelling species occurring in Australia. We measured the reflectance of 1149 specimens from 66 species collected in Australia and Europe, reconstructed a crab spider phylogeny, and applied phylogenetic comparative methods to test our hypotheses. We found that the flower‐dwelling habit evolved independently multiple times, and that this trait was correlated with the evolution of the UV⁺‐white coloration. However, outside Australia non‐flower‐dwelling crab spiders also express a UV⁺‐white coloration. Therefore, UV⁺‐white reflectance is probably a recurring adaptation of some flower dwellers for attracting pollinators, although it may have other functions in non‐flower dwellers, such as camouflage.     

Assassin bug uses aggressive mimicry to lure spider prey

Assassin bugs (Stenolemus bituberus) hunt web-building spiders by invading the web and plucking the silk to generate vibrations that lure the resident spider into striking range. To test whether vibrations generated by bugs aggressively mimic the vibrations generated by insect prey, we compared the responses of spiders to bugs with how they responded to prey, courting male spiders and leaves falling into the web. We also analysed the associated vibrations. Similar spider orientation and approach behaviours were observed in response to vibrations from bugs and prey, whereas different behaviours were observed in response to vibrations from male spiders and leaves. Peak frequency and duration of vibrations generated by bugs were similar to those generated by prey and courting males. Further, vibrations from bugs had a temporal structure and amplitude that were similar to vibrations generated by leg and body movements of prey and distinctly different to vibrations from courting males or leaves, or prey beating their wings. To be an effective predator, bugs do not need to mimic the full range of prey vibrations. Instead bugs are general mimics of a subset of prey vibrations that fall within the range of vibrations classified by spiders as 'prey'.     

Wasp uses venom cocktail to manipulate the behavior of its cockroach prey

The sting of the parasitoid wasp Ampulex compressa is unusual, as it induces a transient paralysis of the front legs followed by grooming behavior and then by a long-term hypokinesia of its cockroach prey. Because the wasp's goal is to provide a living meal for its newborn larva, the behavioral changes in the prey are brought about by manipulating the host behavior in a way beneficial to the wasp and its offspring. To this end, the wasp injects its venom cocktail with two consecutive stings directly into the host's central nervous system. The first sting in the thorax causes a transient front leg paralysis lasting a few minutes. This paralysis is due to the presence of a venom component that induces a postsynaptic block of central cholinergic synaptic transmission. Following the head sting, dopamine identified in the venom appears to induce 30 min of intense grooming. During the long-term hypokinesia that follows the grooming, specific behaviors of the prey are inhibited while others are unaffected. We propose that the venom represses the activity of head ganglia neurons thereby removing the descending excitatory drive to the thoracic neurons.Abbreviations CNS central nervous system - DA dopamine - GI giant interneuron - PSP postsynaptic potential - SEG sub-esophageal ganglion - TI thoracic interneuron     

Carotenoid-based coloration, condition, and immune responsiveness in the nestlings of a sexually dimorphic bird of prey

In many birds, nestlings exhibit brightly colored traits that are pigmented by carotenoids. Carotenoids are diet limited and also serve important health-related physiological functions. The proximate mechanisms behind the expression of these carotenoid-pigmented traits are still poorly known, especially in nestlings with sexual size dimorphism. In these nestlings, intrabrood competition levels and growth strategies likely differ between sexes, and this may in turn influence carotenoid allocation rules. We used dietary carotenoid supplementation to test whether wild marsh harrier (Circus aeruginosus) nestlings were carotenoid limited and whether carotenoid allocation strategies varied between sexes, which differ in their size and growth strategies. When supplemented, nestlings used the supplemental carotenoids to increase their coloration independently of their sex. We showed that the condition dependence of the carotenoid level and the response to an immune challenge (phytohemagglutinin test) differed between sexes, possibly because sexual size dimorphism influences growth strategies and/or intrabrood competition levels and access to different types of food. In this species, which often feeds on mammals, a trade-off likely exists between food quantity (energy) and quality (carotenoid content). Finally, carotenoid-based coloration expressed in marsh harrier nestlings appeared to be indicative of immune responsiveness rather than condition, therefore potentially advertising to parents nestling quality or value rather than nutritional need.     

Background-matching and disruptive coloration, and the evolution of cryptic coloration

Cryptic prey coloration typically bears a resemblance to the habitat the prey uses. It has been suggested that coloration which visually matches a random sample of the background maximizes background matching. We studied this previously untested hypothesis, as well as another, little studied principle of concealment, disruptive coloration, and whether it could, acting in addition to background matching, provide another plausible means of achieving camouflage. We presented great tits (Parus major) with artificial background-matching and disruptive prey (DP), and measured detection times. First, we studied whether any random sample of a background produces equally good crypsis. This turned out to not be the case. Next, we compared the DP and the best background-matching prey and found that they were equally cryptic. We repeated the tests using prey with all the coloration elements being whole, instead of some of them being broken by the prey outline, but this did not change the result. We conclude that resemblance of the background is an important aspect of concealment, but that coloration matching a random visual sample of the background is neither sufficient nor necessary to minimize the probability of detection. Further, our study lends empirical support to the principle of disruptive coloration.     

Great tits (Parus major) searching for artificial prey: implications for cryptic coloration and symmetry

It has been suggested that bilateral symmetry may impose a costfor animals relying on camouflage because symmetric color patternsmight increase the risk of detection. We tested the effect ofsymmetry on crypsis, carrying out a predation experiment withgreat tits (Parus major) and black-and-white–patterned,artificial prey items and background. First, we found that detectiontime was significantly longer for a highly cryptic, asymmetricpattern based on a random sample of the background than forits symmetric variants. Second, we were able to arrange theelements of a prey pattern in a way that the resulting asymmetricpattern was highly cryptic and, furthermore, its symmetric variantwas highly cryptic as well. We conclude that symmetry may imposea substantial cost on cryptic patterns, but this cost variesamong patterns. This suggests that for prey, which predatorstypically view from an angle exposing their symmetry, selectionfor pattern asymmetry may be less important and selection fordecreased detectability cost of symmetry may be more importantthan previously thought. This may help to understand the existenceof so many prey with cryptic, symmetric color patterns.     

Nodal signaling uses activin and transforming growth factor-beta receptor-regulated Smads

Nodal, a member of the transforming growth factor beta (TGF-beta) superfamily, is implicated in many events critical to the early vertebrate embryo, including mesoderm formation, anterior patterning, and left-right axis specification. Here we define the intracellular signaling pathway induced by recombinant nodal protein treatment of P19 embryonal carcinoma cells. Nodal signaling activates pAR3-Lux, a luciferase reporter previously shown to respond specifically to activin and TGF-beta. However, nodal is unable to induce pTlx2-Lux, a reporter specifically responsive to bone morphogenetic proteins. We also demonstrate that nodal induces p(CAGA)(12), a reporter previously shown to be specifically activated by Smad3. Expression of a dominant negative Smad2 significantly reduces the level of luciferase reporter activity induced by nodal treatment. Finally, we show that nodal signaling rapidly leads to the phosphorylation of Smad2. These results provide the first direct biochemical evidence that nodal signaling is mediated by both activin-TGF-beta pathway Smads, Smad2 and Smad3. We also show here that the extracellular cripto protein is required for nodal signaling, making it distinct from activin or TGF-beta signaling.     

Parasitoid wasp uses a venom cocktail injected into the brain to manipulate the behavior and metabolism of its cockroach prey

Unlike other venomous predators, the parasitoid wasp Ampulex compressa incapacitates its prey, the cockroach Periplaneta americana, to provide a fresh food supply for its offspring. We first established that the wasp larval development, from egg laying to pupation, lasts about 8 days during which the cockroach must remain alive but immobile. To this end, the wasp injects a cocktail of neurotoxins to manipulate the behavior of the cockroach. The cocktail is injected directly into the head ganglia using biosensors located on the stinger. The head sting induces first 30 min of intense grooming followed by hypokinesia during which the cockroach is unable to generate an escape response. In addition, stung cockroaches survive longer, lose less water, and consume less oxygen. Dopamine contained in the venom appears to be responsible for inducing grooming behavior. For the hypokinesia, our hypothesis is that the injected venom affects neurons located in the head ganglia, which send descending tonic input to bioaminergic neurons. These, in turn, control the thoracic premotor circuitry for locomotion. We show that the activity of identified octopaminergic neurons from the thoracic ganglia is altered in stung animals. The alteration in the octopaminergic neurons' activity could be one of the mechanisms by which the venom modulates the escape circuit in the cockroach's central nervous system and metabolism in the peripheral system.     

Habitat structure and prey composition generate contrasting effects on carotenoid‐based coloration of great tit Parus major nestlings

Carotenoid‐based coloration of nestling plumage is generally considered a reliable signal of quality and has consistently been related to habitat structure. The main hypothesis proposed to explain this correlation is that high quality habitats contain high quality food, which in return affects the expression of carotenoid‐based plumage. It therefore assumes that, at the population level, the link between habitat structure and food composition is consistent and more relevant than inter‐individual differences in foraging ability or parental investment. In addition, it is assumed by default that food and habitat produce concordant effects on nestling coloration. In this work we evaluated habitat structure and prey composition in addition to several measures of parental investment. We investigated their relative effect on carotenoid‐based plumage coloration (lightness, chroma and hue) of great tit Parus major nestlings. We found a low correlation between carotenoid‐based coloration of nestlings and that of their parents. Nestling coloration, especially lightness and chroma, increased with the intake of more spiders. The time of breeding was positively correlated with lightness and chroma and negatively correlated with hue. Finally, the maturity of oak trees surrounding nest‐boxes correlated negatively with lightness, and the size of all tree species surrounding nest‐boxes correlated positively with hue of chick plumage. Our findings support the view that habitat structure and prey composition may produce divergent effects on feather pigmentation, and that prey proportions and variables related to parental investment should be assessed when considering carotenoid‐based coloration of chicks. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 547–555.     

Antagonistic evolution in an aposematic predator–prey signaling system

Warning signals within species, such as the bright colors of chemically defended animals, are usually considered mutualistic, monomorphic traits. Such a view is however increasingly at odds with the growing empirical literature, showing nontrivial levels of signal variation within prey populations. Key to understanding this variation, we argue, could be a recognition that toxicity levels frequently vary within populations because of environmental heterogeneity. Inequalities in defense may undermine mutualistic monomorphic signaling, causing evolutionary antagonism between loci that determine appearance of less well‐defended and better defended prey forms within species. In this article, we apply a stochastic model of evolved phenotypic plasticity to the evolution of prey signals. We show that when toxicity levels vary, then antagonistic interactions can lead to evolutionary conflict between alleles at different signaling loci, causing signal evolution, “red queen‐like” evolutionary chase, and one or more forms of signaling equilibria. A key prediction is that variation in the way that predators use information about toxicity levels in their attack behaviors profoundly affects the evolutionary characteristics of the prey signaling systems. Environmental variation is known to cause variation in many qualities that organisms signal; our approach may therefore have application to other signaling systems.