Aposematic coloration, luminance contrast, and the benefits of conspicuousness

Many organisms use warning, or aposematic, coloration to signaltheir unprofitability to potential predators. Aposematicallycolored prey are highly visually conspicuous. There is considerableempirical support that conspicuousness promotes the effectivenessof the aposematic signal. From these experiments, it is welldocumented that conspicuous, unprofitable prey are detectedsooner and aversion learned faster by the predator as comparedwith cryptic, unprofitable prey. Predators also retain memoryof the aversion longer when prey is conspicuous. The presentstudy focused on the elements of conspicuousness that conferthese benefits of aposematic coloration. Drawing on currentunderstanding of animal vision, we distinguish 2 features ofwarning coloration: high chromatic contrast and high brightness,or luminance, contrast. Previous investigations on aposematicsignal efficacy have focused mainly on the role of high chromaticcontrast between prey and background, whereas little researchhas investigated the role of high luminance contrast. Usingthe Chinese mantid as a model predator and gray-painted milkweedbugs as model prey, we found that increased prey luminance contrastincreased detection of prey, facilitated predator aversion learning,and increased predator memory retention of the aversive response.Our results suggest that the luminance contrast component ofaposematic coloration can be an effective warning signal betweenthe prey and predator. Thus, warning coloration can even evolveas an effective signal to color blind predators.     

The effect of metapopulation dynamics on the survival and spread of a novel, conspicuous prey

Animals that deploy chemical defences against predators often signal their unprofitability using bright colouration. This pairing of toxicity and conspicuous patterning is known as aposematism.Explaining the evolution and spread of aposematic traits in previously cryptic species has been the focus of much empirical and theoretical work over the last two decades. Existing research concerning the initial evolution of aposematism does not however properly consider that many aposematic species (such as members of the hymenoptera, the lepidoptera, and amphibia) are highly mobile. We argue in this paper that the evolution of aposematic displays is therefore often best understood within a metapopulation framework; hence in this paper we present the first explicit metapopulation model of the evolution of aposematism. Our most general finding is that migration tends to reduce the probability that an aposematic prey can increase from rarity and spread across a large population. Hence, the best case scenarios for the spread of aposematism required fixation of the aposematic form in one or more isolated sub-habitats prior to some event which subsequently enabled migration. We observed that changes in frequency of new aposematic forms within source habitats are likely to be nonmonotonic. First, aposematic prey tend to decline in frequency as they migrate outwards from the source habitat to neighbouring sink habitats, but subsequently they increase in relative abundance in the source, as the descendents of earlier migrants migrate back from newly converted sub-populations. This pattern of initial loss and subsequent gain between new source and neighbouring sink habitats is then repeated as the aposematic form spreads via a moving cline.     

Adaptive coloration, behavior and predation vulnerability in three juvenile north Pacific flatfishes

Adaptive color change in flatfish has long been of interest to scientists, yet rarely studied from an ecological perspective. Because color change can take a day or so in some species, movement between sediments with differing color or texture may render fish more conspicuous to predators. We conducted laboratory experiments to test the following hypotheses related to adaptive color change in flatfish: 1) fish which do not cryptically match sediment will be more vulnerable to predation, 2) fish will reduce activity and bury to minimize conspicuousness when on a sediment they mismatch, and 3) fish will choose a sediment they match when given a choice. Experiments were conducted using three co-occurring north Pacific juvenile flatfishes: English sole Parophrys vetulus, northern rock sole Lepidopsetta polyxystra and Pacific halibut Hippoglossus stenolepis. As per expectations, juvenile flatfish were more vulnerable to visual predators when they mismatched sediment. Mismatched fish tended to behave differently than fish which matched the sediment. Rather than burying and becoming inactive, they became more active and less likely to bury, perhaps contributing to their predation vulnerability. This increased activity may have represented search for better matching sediment, a stress response, or conspicuousness-related density dependent behavior. Fish which had acclimated to light colored sediment preferred light over dark sediment in choice trials. In contrast, fish acclimated to dark sediment demonstrated no preference. These experiments demonstrate that adaptive coloration is an integral part of the flatfish detection minimization strategy and that movement between habitats can increase risk of predation.     

The evolution of locomotory behavior in profitable and unprofitable simulated prey

Prey that are unprofitable to attack (for example, those containing noxious chemicals) frequently exhibit slower and more predicable movement than species that lack these defenses. Possible explanations for the phenomenon include a lack of selection pressure on unprofitable prey to avoid predators and active selection on unprofitable prey to advertise their noxiousness. We explicitly tested these and other hypotheses using a novel artificial world in which the locomotory characteristics (step size, waiting time, and angular direction) of artificial profitable and unprofitable computer-generated prey were subject to continued selection by humans over a number of generations. Unprofitable prey evolved significantly slower movement behavior than profitable prey when they were readily recognized as unprofitable, and also when they frequently survived predatory attacks. This difference arose primarily as a consequence of more intense selection on profitable prey to avoid capture. When unprofitable prey were very similar (but not identical) in morphological appearance to profitable prey, unprofitable prey evolved particularly slow movement behavior, presumably because when they were slow-moving they could be more readily recognized as being unprofitable. When unprofitable prey were constrained to move slowly, a morphologically identical profitable prey species evolved locomotor mimicry only when it had no more effective means of avoiding predation. Overall, our results provide some of the first empirical support for a number of earlier hypotheses for differences in movement between unprofitable and profitable prey and demonstrate that locomotor mimicry is not an inevitable outcome of selection even in morphologically similar prey.     

Quantifying two-dimensional dichromatic patterns using a photographic technique: case study on the shore crab (<Emphasis Type="Italic">Carcinus maenas</Emphasis> L.)

Contrasting patterns of pigmentation, such as those associated with crypsis and aposematism, are common in many taxa. In order to determine why patterning varies among individuals or populations, it is important to quantify how these patches of pigment are arranged. Here we present a simple technique for measuring areas of pigmentation as well as their spatial distribution, and demonstrate its application to the study of substrate-associated patterning in shore crabs (Carcinus maenas L.). The results, based on a virtual grid laid over digital images of crab carapaces, allow for correlations to be made among sample populations. The technique, or variations of it, can be applied to any situation where two-dimensional dichromatic patterns need to be quantified.     

Predator mixes and the conspicuousness of aposematic signals

Conspicuous warning signals of unprofitable prey are a defense against visually hunting predators. They work because predators learn to associate unprofitability with bright coloration and because strong signals are detectable and memorable. However, many species that can be considered defended are not very conspicuous; they have weak warning signals. This phenomenon has previously been ignored in models and experiments. In addition, there is significant within- and among-species variation among predators in their search behavior, in their visual, cognitive, and learning abilities, and in their resistance to defenses. In this article we explore the effects of variable predators on models that combine positive frequency-dependent, frequency-independent, and negative frequency-dependent predation and show that weak signaling of aposematic species can evolve if predators vary in their tendency to attack defended prey.     

Evolutionary implications of deception in mimicry and masquerade

Aggressive mimicry occurs when an organism resembles some aspect of another organism （the model） in order to obtain prey through its deceptive resemblance. This may function either through the overt response of the receiver or through the lack of response of the receiver. Reviewing selected examples, I discuss some of the difficulties in ascribing a model for the mimic. I also discuss how a single animal can have multiple ploys in its armoury of deceptive signals, thus belonging within two or more categories of deceptive signalling. In addition to aggressive mimicry, these may include crypsis or camouflage, mas- querade （mimicry of inanimate objects）, and Batesian or protective mimicry. Each of these examples of deception has multiple evolutionary pathways, and some deceptive signals may be more costly to receivers than others, but no single organism is subject to a single selection pressure, leading to the reality that many evolutionary pathways contribute to the diversity we see around us. New technologies are opening new channels of investigation into deceptive signaling in many different sensory modalities, and this is reflected in the recent increase in studies investigating the structure and function of deceptive signals. In turn, these studies are beginning to expose the fascinating complexity of deceptive signaling systems, allowing us to discover the myriad, non-mutually exclusive, solutions that can be selected for to obtain prey     

Identifying the ecological conditions that select for intermediate levels of aposematic signalling

Chemically defended species often have conspicuous signals that warn potential predators of these defences. Recent evidence suggests that some such aposematic prey are not as conspicuous as possible, even though increased conspicuousness would bring additional anti-predator benefits. Here we present a simple model to explore the generality of these observations. Our model predicts that optimal fitness will often be achieved at an intermediate level of conspicuousness and not simply by maximising conspicuousness. This comes about because of the ubiquitous trade-off that increased conspicuousness has an ecological cost in increasing the encounter rate with predators, as well as a benefit in terms of enhancing learned aversion by predators of defended prey. However, importantly, we also predict that a small deviation away from maximal crypsis generally causes a decrease in fitness, even if a larger deviation would lead to an intermediate level of conspicuousness that maximises fitness. Hence, further consideration of whether intermediate levels of aposematism are as common in nature as predicted in this model will require consideration of the underlying evolution of appearance, and the plausibility of evolution across the fitness trough, from maximal crypsis to an intermediate level of aposematism.     

Predictors of orbital convergence in primates: a test of the snake detection hypothesis of primate evolution

Traditional explanations for the evolution of high orbital convergence and stereoscopic vision in primates have focused on how stereopsis might have aided early primates in foraging or locomoting in an arboreal environment. It has recently been suggested that predation risk by constricting snakes was the selective force that favored the evolution of orbital convergence in early primates, and that later exposure to venomous snakes favored further degrees of convergence in anthropoid primates. Our study tests this snake detection hypothesis (SDH) by examining whether orbital convergence among extant primates is indeed associated with the shared evolutionary history with snakes or the risk that snakes pose for a given species. We predicted that orbital convergence would be higher in species that: 1) have a longer history of sympatry with venomous snakes, 2) are likely to encounter snakes more frequently, 3) are less able to detect or deter snakes due to group size effects, and 4) are more likely to be preyed upon by snakes. Results based on phylogenetically independent contrasts do not support the SDH. Orbital convergence shows no relationship to the shared history with venomous snakes, likelihood of encountering snakes, or group size. Moreover, those species less likely to be targeted as prey by snakes show significantly higher values of orbital convergence. Although an improved ability to detect camouflaged snakes, along with other cryptic stimuli, is likely a consequence of increased orbital convergence, this was unlikely to have been the primary selective force favoring the evolution of stereoscopic vision in primates.     

The relationship between habitat structure and fish faunas on New Zealand reefs

Reef fish abundances were sampled at 11 shallow reef localities extending over 1000 km of coastline in northern New Zealand. Sampling was restricted to the 4–10-m depth stratum and included six coastal and five island localities. These were either coralline reef flats dominated by echinoids, or algal reefs with high densities of laminarian and fucoid algae. Reefs dominated by macroscopic algae supported large numbers of small fishes, mainly labrids, and few large benthic-feeding fishes. Echinoid-dominated reefs supported a different fish fauna with more large benthic-feeding species. Additional sampling of echinoiddominated reefs and algal stands in deeper water provided confirmation of these findings. A second sampling programme was carried out at a series of eight sites within a single locality covering 5 km of coastline. These spanned a moderate exposure gradient and ranged from algal dominated reefs to typical coralline reef flats with high densities of grazing invertebrates. The relationship between habitat structure and reef fish species composition and size frequency was similar to that of the large-scale sampling programme. Thirdly, observations on reef fish foraging and feeding patterns within a single reef site suggested that larger benthic-feeding reef fishes were less likely to feed within macroscopic algal stands. Experimental reductions of grazing invertebrates designed to produce brown algal stands on echinoid-dominated reef flats supported these observations. Larger individuals capable of removing echinoids and grazing gastropods did not frequent or feed in laminarian and fucoid algal stands. This pattern is discernible at several spatial scales. Our conclusion is that the type of shallow reef habitat, echinoid- as opposed to algal-dominated, will have an important rôle in determining the associated reef fish fauna.     

Sex differences but no evidence of quantitative honesty in the warning signals of six‐spot burnet moths (Zygaena filipendulae L.)*

The distinctive black and red wing pattern of six‐spot burnet moths (Zygaena filipendulae, L.) is a classic example of aposematism, advertising their potent cyanide‐based defences. While such warning signals provide a qualitatively honest signal of unprofitability, the evidence for quantitative honesty, whereby variation in visual traits could provide accurate estimates of individual toxicity, is more equivocal. Combining measures of cyanogenic glucoside content and wing color from the perspective of avian predators, we investigate the relationship between coloration and defences in Z. filipendulae, to test signal honesty both within and across populations. There were no significant relationships between mean cyanogenic glucoside concentration and metrics of wing coloration across populations in males, yet in females higher cyanogenic glucoside levels were associated with smaller and lighter red forewing markings. Trends within populations were similarly inconsistent with quantitative honesty, and persistent differences between the sexes were apparent: larger females, carrying a greater total cyanogenic glucoside load, displayed larger but less conspicuous markings than smaller males, according to several color metrics. The overall high aversiveness of cyanogenic glucosides and fluctuations in color and toxin levels during an individual's lifetime may contribute to these results, highlighting generally important reasons why signal honesty should not always be expected in aposematic species.     

Evolutionary constraints of warning signals: A genetic trade‐off between the efficacy of larval and adult warning coloration can maintain variation in signal expression

To predict evolutionary responses of warning signals under selection, we need to determine the inheritance pattern of the signals, and how they are genetically correlated with other traits contributing to fitness. Furthermore, protective coloration often undergoes remarkable changes within an individual's lifecycle, requiring us to quantify the genetic constraints of adaptive coloration across all the relevant life stages. Based on a 12 generation pedigree with > 11,000 individuals of the wood tiger moth (Arctia plantaginis), we show that high primary defense as a larva (large warning signal) results in weaker defenses as adult (less efficient warning color), due to the negative genetic correlation between the efficacy of larval and adult warning coloration. However, production of effective warning coloration as a larva did not incur any life‐history costs and was positively genetically correlated with reproductive output. These results provide novel insights into the evolutionary constraints on protective coloration in animals, and explain the maintenance of variation in the signal expression despite the strong directional selection by predators. By analyzing the genetic and environmental effects on warning signal and life‐history traits in all relevant life stages, we can accurately determine the mechanisms shaping the evolutionary responses of phenotypic traits under different selection environments.     

Warning signals are seductive: Relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies

Visual signaling in animals can serve many uses, including predator deterrence and mate attraction. In many cases, signals used to advertise unprofitability to predators are also used for intraspecific communication. Although aposematism and mate choice are significant forces driving the evolution of many animal phenotypes, the interplay between relevant visual signals remains little explored. Here, we address this question in the aposematic passion‐vine butterfly Heliconius erato by using color‐ and pattern‐manipulated models to test the contributions of different visual features to both mate choice and warning coloration. We found that the relative effectiveness of a model at escaping predation was correlated with its effectiveness at inducing mating behavior, and in both cases wing color was more predictive of presumptive fitness benefits than wing pattern. Overall, however, a combination of the natural (local) color and pattern was most successful for both predator deterrence and mate attraction. By exploring the relative contributions of color versus pattern composition in predation and mate preference studies, we have shown how both natural and sexual selection may work in parallel to drive the evolution of specific animal color patterns.     

The interrelationship between crypsis and colour polymorphism

The mechanisms behind the evolution and maintenance of conspicuous visible polymorphisms comprising tens of morphs present a challenge to evolutionary theory. However, for cryptic forms Endler (Evol. Biol., 11, 1978, 319) conjectured that complex backgrounds facilitate polymorphism because in such habitats there are several ways to resemble the resting surface. We use computer simulation to explore the evolution of cryptic morphs on increasingly complex backgrounds under regimes that include selection for crypsis, apostatic predation and dietary wariness. We show that there is a monotonic increase in the number of morphs evolving in a population as the potential number of cryptic morphs increases. The relationship is very weak with selection for crypsis alone, but much stronger with the addition of apostatic selection. In contrast, when dietary wariness is added to the model the plot of number of morphs maintained, as a function of the potential number of cryptic forms available, is minimized at an intermediate number of cryptic forms, i.e. is V-shaped. These counter-intuitive patterns are robust to varying strengths of apostatic selection and different implementations of dietary wariness, and are more pronounced when predator and prey generation lengths are similar.     

The relationship between wound-induced proteinase inhibitors and hydraulic signals in tomato seedlings

Localized wounding is known to induce systemic proteinase inhibitors (PI) in seedlings of tomato (Lycopersicon esculentum L.). Inhibitors of elastase (EC 3.4.21.36) were shown here to be among those systemically induced by wounding, and a simple rapid assay for PI based on elastase was developed. Using this assay, the nature of the systemic signalling system (‘PIIF’) was investigated. Hydraulic signals were shown to be induced in tomato by localized wounds. These signals travelled throughout the plant well within the lag time before appearance of systemic wound-induced PI. A number of correlations were drawn between the occurrence of the hydraulic signals and induction of systemic PI, suggesting that hydraulic signals might be the PIIF, or a component of it. It was shown that systemic hydraulic signals could be triggered, without significant wounding, by excision of a single leaflet through the submerged petiole. These hydraulic signals were similar in both kinetics and magnitude to those induced by localized wounding. However, they did not induce systemic PI. In addition, it was shown that systemic events almost as rapid as wound-induced hydraulic signals could be induced without wounding, under certain environmental conditions. This indicates that rapid hydraulic signals do not provide a specific signal of wounding. These findings demonstrate that hydraulic signals per se are not the PIIF.     

Using the angle frequency method to detect signals of competition and predation in experimental time series

Identifying interactions among organisms is central to the study of ecology. The Angle Frequency Method (AFM) allows the detection of interactions in time series data. The AFM takes pairwise data plotted in phase diagrams and identifies signals (vector directions in phase diagrams) associated with particular interactions. Using microbial experimental systems consisting of predators (bacteriophage T4) and prey/competitors (strains of Escherichia coli), we demonstrate that the AFM can identify predator–prey and competitive interactions. The level of control afforded by such microbial experimental systems allows direct tests of the utility and robustness of the AFM. Signals of predation were distinct from signals of competition, with the strongest signal of predation corresponding to the collapse of the predator population at low prey densities. Signals of competition reflected the difference in competitive strength between the superior and the inferior competitors. In addition, the effects of invasion and resource enrichment on interactions in the laboratory communities were detectable using the AFM. Our analyses support results from model simulations and analyses of lake time series by identifying similar sets of signals characteristic of predation and competition, and demonstrate that the AFM is an effective tool in rigorous studies of time series.     

Field observation on death feigning: a unique hunting behavior by the predatory cichlid,Haplochromis livingstoni,of Lake Malawi

Synopsis Haplochromis (=Cyrtocara) livingstoni, one of the predatory cichlids of the sand community of Lake Malawi, Africa, occurs at a density of 1.3 individuals per hectare. They are territorial, defending areas 15 m wide by 40 m long along the interface of sand andVallisneria weed beds. Individuals use a death feigning hunting pattern to capture prey. From a position of lying on their sides semiburied in the sand, these fish attack small cichlids. During four hours of SCUBA observations three successful attacks from this position were seen. After an attack the small cichlids scatter and the predator moves on toward a new aggregation of fish where it again plays dead. Individuals feign death an average of seven times per thirty minutes watch. Death feigning behavior is initiated in two ways. The fish either 1) is stationary with its ventral surface on or close to the sand, and then falls onto its side, or 2) drops from the water colum into `lying on side' position. The initial behavioral actions of the latter method are similar to chafing behavior. But instead of chafing the sand and rising again off the bottom, the fish plows into the sand and remains immobile. These data further add to the evidence that cichlids are remarkably flexible in their feeding behavior.     

Zebra stripes and tiger stripes: the spatial frequency distribution of the pattern compared to that of the background is significant in display and crypsis

Some striped animals are camouflaged in their natural environment, whereas others are conspicuous. Mammals are known to have spatial frequency analysers in their visual mechanism, and it is suggested that the spatial characteristics of a striped pattern are different in camouflaged and conspicuous animals. Fourier analysis of the stripes of the zebra shows spatial frequencies in the pattern that are unlikely to be present so strongly in their natural background scene. A similar analysis of the camouflaging stripes of a tiger show that the distribution of spatial frequencies are similar to that in the background scene.     

A recombinant diheme SoxAX cytochrome - implications for the relationship between EPR signals and modified heme-ligands

The multiheme SoxAX proteins are notable for their unusual heme ligation (His/Cys-persulfide in the SoxA subunit) and the complexity of their EPR spectra. The diheme SoxAX protein from Starkeya novella has been expressed using Rhodobacter capsulatus as a host expression system. rSoxAX was correctly formed in the periplasm of the host and contained heme c in similar amounts as the native SoxAX. ESI-MS showed that the full length rSoxA, in spite of never having undergone catalytic turnover, existed in several forms, with the two major forms having masses of 28687 +/- 4 and 28718 +/- 4 Da. The latter form exceeds the expected mass of rSoxA by 31 +/- 4 Da, a mass close to that of a sulfur atom and indicating that a fraction of the recombinant protein contains a cysteine persulfide modification. EPR spectra of rSoxAX contained all four heme-dependent EPR signals (LS1a, LS1b, LS2, LS3) found in the native SoxAX proteins isolated from bacteria grown under sulfur chemolithotrophic conditions. Exposure of the recombinant SoxAX to different sulfur compounds lead to changes in the SoxA mass profile as determined by ESI while maintaining a fully oxidized SoxAX visible spectrum. Thiosulfate, the proposed SoxAX substrate, did not cause any mass changes while after exposure to dimethylsulfoxide a +112 +/- 4 Da form of SoxA became dominant in the mass spectrum.