Adaptive change in protective coloration in adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae): test of detectability of two colour forms by avian predators

1. Protective coloration in insects may be aposematic or cryptic, and some species change defensive strategy between instars. In Sweden, the adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae) undergo a seasonal colour change from pale brown and black striation in the pre‐hibernating adults, to red and black striation in the same post‐hibernating individuals. To the human eye the pre‐hibernating adults appear cryptic against the withered late summer vegetation, whereas the red and black post‐hibernating adults appear aposematic. This suggests a possibility of a functional colour change. However, what is cryptic to the human eye is not necessarily cryptic to a potential predator. 2. Therefore we tested the effect of coloration in adult G. lineatum on their detectability for avian predators. Great tits (Parus major) were trained to eat sunflower seeds hidden inside the emptied exoskeletons of pale or red G. lineatum. Then the detection time for both colour forms was measured in a dry vegetation environment. 3. The birds required a longer time to find the pale form of G. lineatum than the red one. The pale form appears more cryptic on withered late summer vegetation than the red form, not only to the human eye but also to avian predators. The result supports the idea that the adult individuals of G. lineatum undergo a functional change from a cryptic protective coloration to an aposematic one.     

Higher survival of an aposematic than of a cryptic form of a distasteful bug

Summary An experiment was performed to assess the relative survival of two forms of 5th instar larvae of Lygaeus equestris (Heteroptera, Lygaeidae) — the normal red form, called aposematic, and a mutant grey form, called cryptic — when given to hand-raised great tits (Parus major).Sixteen birds were presented with aposematic larvae and 16 were presented with cryptic larvae in 10 consecutive trials. One attack per trial was allowed. Both larval forms were presented against a background matching the grey larvae, but since both prey types were presented in a specific place known to the predator, detection rate for both was assumed to be unity.Birds learned to avoid both prey types. However, the survival of the aposematic larvae was higher than that of the cryptic ones due to three aspects of predator behaviour: i) a greater initial reluctance to attack, ii) a more rapid avoidance learning, and iii) a lower frequency of killing in an attack, when the prey was aposematic. Moreover, a greater number of birds learned to avoid prey without killing any individual, when the prey was aposematic. This result is considered to be due to prey coloration alone, since, in a separate test, no difference in prey distastefulness could be detected.This experiment shows that individual prey can benefit from being aposematic and indicates that individual selection can be a sufficient explanation for the evolution of aposematic coloration. It was concluded that, since the survivorship was 6.4 times higher for the aposematic prey, it could have a detection rate that is correspondingly higher than the cryptic in order for the two forms to have equal fitness.     

Experienced chicks show biased avoidance of stronger signals: an experiment with natural colour variation in live aposematic prey

An important factor for understanding the evolution of warning coloration in unprofitable prey is the synergistic effect produced by predator generalisation behaviour. Warning coloration can arise and become stabilised in a population of solitary prey if more conspicuous prey benefit from a predator's previous interaction with less conspicuous prey. This study investigates whether domestic chicks (Gallus gallus domesticus) show a biased generalisation among live aposematic prey by using larvae of three species of seed bugs (Heteroptera: Lygaeidae) that are of similar shape but vary in the amount of red in the coloration. After positive experience of edible brownish prey, chicks in two reciprocal experiments received negative experience of either a slightly red or a more red distasteful larva. Attacking birds were then divided into two treatment groups, – one presented with the same prey again, and one presented with either a less red or a more red larva. Birds with only experience of edible prey showed no difference in attack probability of the two aposematic prey types. Birds with experience of the less red prey biased their avoidance so that prey with a more red coloration was avoided to a higher degree, whereas birds with experience of the more red prey avoided prey with the same, but not less red coloration. Thus, we conclude that bird predators may indeed show a biased generalisation behaviour that could select for and stabilise an aposematic strategy in solitary prey. This revised version was published online in July 2006 with corrections to the Cover Date.     

Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence

Many aposematic species have evolved an aggregated lifestyle, and one possible advantage of grouping in warningly coloured prey is that it makes the aposematic signal more effective by generating a greater aversion in predators. Here we investigate the effect of prey group size on predator behaviour, both when prey are aposematic and when they are not aposematic, to separate the effects of warning coloration and prey novelty. Naive domestic chicks (Gallus gallus domesticus) were presented with either solitary or groups of 3, 9 or 27 live larvae of the aposematic bug Tropidothorax leucopterus. Other naive chicks were presented with larvae of the non-aposematic bug Graptostethus servus either solitary or in groups of 27. Attack probability decreased with increasing group size of aposematic prey, both when birds were naive and when they had prior experience, whereas prey gregariousness did not affect the initial attack probability on the G. servus larvae. In a separate experiment, groups of mealworms were shown to be even more attractive than solitary mealworms to naive chicks. We conclude that the aversiveness of prey grouping in this study can be explained as increased signal repellence of specific prey coloration, in this case a classical warning coloration. These experiments thus support the idea of gregariousness increasing the signalling effect of warning coloration.     

Investigating the behavioral significance of color pattern in a cichlid fish: firemouths <Emphasis Type="Italic">Thorichthys meeki</Emphasis> respond differently to color-manipulated video and dummy conspecifics

Red coloration is a conspicuous feature of many visual signals and can function to attract or deter its viewers. Among fishes, red is associated with specialized nuptial, territorial and aposematic (warning) displays. Both sexes of the firemouth cichlid fish Thorichthys meeki develop red ventral coloration at sexual maturity, along with temporally variable black (melanic) elements. Isolated adult firemouth cichlids sequentially presented paired dummy and paired video conspecifics, both with and without red ventral coloration. Subjects interacted more with red-containing stimuli, but with a significant interaction: dummy presentations revealed a strong, positive red bias that video presentations did not. In addition, the melanic color pattern displayed by subjects at the initiation of each trial had a significant effect on subject responsiveness. These results reveal the potential for between-subject differences and experimental design parameters to interact critically in the study of animal color patterns.     

Teasing apart crypsis and aposematism – evidence that disruptive coloration reduces predation on a noxious toad

Both cryptic and aposematic colour patterns can reduce predation risk to prey. These distinct strategies may not be mutually exclusive, because the impact of prey coloration depends on a predator's sensory system and cognition and on the environmental background. Determining whether prey signals are cryptic or aposematic is a prerequisite for understanding the ecological and evolutionary implications of predator–prey interactions. This study investigates whether coloration and pattern in an exceptionally polymorphic toad, Rhinella alata, from Barro Colorado Island, Panama reduces predation via background matching, disruptive coloration, and/or aposematic signaling. When clay model replicas of R. alata were placed on leaf litter, the model's dorsal pattern – but not its colour – affected attack rates by birds. When models were placed on white paper, patterned and un‐patterned replicas had similar attack rates by birds. These results indicate that dorsal patterns in R. alata are functionally cryptic and emphasize the potential effectiveness of disruptive coloration in a vertebrate taxon.     

Carotenoid-based colour polyphenism in a moth species: search for fitness correlates

Carotenoid‐based integumental coloration is often associated with individual performance in various animals. This is because the limited amount of the pigment has to be allocated to different vital functions. However, most of the evidence for the carotenoid‐based trade‐off comes from vertebrate studies, and it is unclear if this principle can be applied to insects. This possibility was investigated in Orgyia antiqua L. (Lepidoptera: Lymantriidae). The larvae of this species are polyphenic in their coloration, varying from a highly conspicuous combination of yellow hair tufts on black background to cryptic appearance with brown hair tufts. The conspicuous larvae are aposematic, advertising their aversive hairiness. The maintenance of different colour morphs in O. antiqua requires explanation, as an aposematic signal is expected to evolve towards monomorphism. Chromatographic analysis showed that the yellow coloration of the hair is based on the carotenoid pigment lutein (α‐carotene‐3,3’‐diol). The colour of hair tufts was dependent on their carotenoid content. This justifies an expectation of carotenoid‐based physiological trade‐offs between aposematic coloration and individual performance. To test this hypothesis, we monitored life histories of differently coloured larvae reared on various host plants, recording their body sizes, growth rates, and mortalities in each instar. There was a significant but relatively low heritability of tuft coloration, which allowed us to expect environmental effects. We found no phenotypic associations between hair tuft colour and performance indices in O. antiqua larvae, neither did the quality of host plant affect the frequency of colour morphs. However, the frequency of colour morphs differed between larval instars. Our results suggest that carotenoid‐mediated physiological trade‐offs are not involved in the maintenance of colour morphs in O. antiqua larvae, and factors other than individual condition should be responsible for the observed variability.     

Reactions of green lizards (Lacerta viridis) to major repellent compounds secreted by Graphosoma lineatum (Heteroptera: Pentatomidae)

The chemical defence of Heteroptera is primarily based on repellent secretions which signal the potential toxicity of the bug to its predators. We tested the aversive reactions of green lizards (Lacerta viridis) towards the major compounds of the defensive secretion of Graphosoma lineatum, specifically: (i) a mixture of three aldehydes: (E)-hex-2-enal, (E)-oct-2-enal, (E)-dec-2-enal; (ii) a mixture of these three aldehydes and tridecane; (iii) oxoaldehyde: (E)-4-oxohex-2-enal; (iv) secretion extracted from metathoracic scent glands of G. lineatum adults and (v) hexane as a non-polar solvent. All chemicals were presented on a palatable food (Tenebrio molitor larvae). The aversive reactions of the green lizards towards the mealworms were evaluated by observing the approach latencies, attack latencies and approach–attack intervals. The green lizards exhibited a strong aversive reaction to the mixture of three aldehydes. Tridecane reduced the aversive reaction to the aldehyde mixture. Oxoaldehyde caused the weakest, but still significant, aversive reaction. The secretion from whole metathoracic scent glands also clearly had an aversive effect on the green lizards. Moreover, when a living specimen of G. lineatum or Pyrrhocoris apterus (another aposematic red-and-black prey) was presented to the green lizards before the trials with the aldehyde mixture, the aversive effect of the mixture was enhanced. In conclusion, the mixture of three aldehydes had the strong aversive effect and could signal the potential toxicity of G. lineatum to the green lizards.     

The evolution of conspicuous coloration: Some experiments in bad taste

Unpalatable species are often brightly coloured. Such aposematic coloration may have evolved because predators can learn to avoid conspicuous prey more readily than cryptic prey. Experiments on young male chicks are described and the results are consistent with this hypothesis.     

Field but not lab paradigms support generalisation by predators of aposematic polymorphic prey: the Oophaga histrionica complex

The persistence of novel aposematic forms, and thereby the evolution of aposematic polymorphism, remain intriguing. Novel and rare forms could be disproportionally attacked by predators that already learned to avoid a pre-existing and more common aposematic form. Alternatively, novel forms could be less frequently attacked if predators are reluctant to attack unknown potential prey (neophobia) or if previous learning allows them to generalise and recognise the novel form as toxic. We used colour variation in polymorphic poison frogs (Oophaga histrionica complex) to test whether predators familiar with one aposematic form do generalise their avoidance behaviour to other aposematic forms. To strengthen our inference, we combined a field test of attack rates to local and non-local models with a lab experiment of generalisation capabilities by newly born chicks. Field predators attacked a significantly lower proportion of 529 aposematic compared to 150 cryptic models. Predators co-occurring with the local aposematic form of O. histrionica equally avoided non-local forms, especially in areas where the species was abundant. Forty-two lab chicks learned to discriminate between an aposematic and a cryptic image, but failed to generalise to other aposematic images, even though we tried with six combinations of aposematic forms. To better mimic the situation in the field, we further tested whether chicks trained with a set of four simultaneous aposematic images would generalise better. They failed to learn the discrimination task. Our data contrast with previous field studies on other poison frogs, and support a role for generalisation, and arguably not neophobia, in predator avoidance of novel aposematic forms.     

The effects of background coloration and dark spots on the risk of predation in poison frog models

Protective coloration is a well-known predator avoidance strategy in prey species. Aposematic species often display a contrasting color pattern consisting of dark spots of different shapes and sizes on a bright background coloration. Both elements, background color and spots are expected to serve different purposes. While the ecological function of the bright coloration has been addressed in many studies, the question of whether the interaction with differently sized spots influences predator behavior has received less attention by researchers. In a lowland rain forest in Costa Rica we used 2700 clay models that imitated the polytypic strawberry poison frog (Oophaga pumilio) as a proxy for an aposematic prey species. We manipulated the dorsal color pattern by using a local and a non-local aposematic and a non-local cryptic background color and combined them with black spots increasing in size (none, small, medium, large). The major objective was to test if spot size alters the survival rate of differently colored models. Background coloration and spot size were significant predictors of being attacked. However, the interaction between both effects was not. During five trials predators avoided the non-local aposematic color morph and did not discriminate between local aposematic and non-local cryptic models. Spot size and attack rate were negatively linear correlated which suggests that predator selection promotes the evolution of dark spots. We further conclude that spot size matters in a contrasting color pattern and plays an important role in predator avoidance.     

Aposematic coloration does not deter corallivory by fish on the coral <Emphasis Type="Italic">Montastraea cavernosa</Emphasis>

Predation on corals by visual predators is a significant source of partial or total mortality on coral reefs, and corals have evolved strategies, including chemical defenses, to deter predation. One mechanism that organisms use to communicate the presence of chemical defenses is aposematic coloration, or the display of bright coloration as a warning to visual predators such as fish. Corals exhibit multiple colors, and it has been hypothesized that one role for this variability in coloration is as an aposematic warning of adverse palatability. Here, we test green and orange color morphs of the Caribbean coral Montastraea cavernosa for the presence of chemical defenses and whether their differences in coloration elicited different feeding responses. While M. cavernosa is chemically defended, there is no difference in feeding deterrence between color morphs; thus, the different color morphs of this coral species do not appear to represent an example of aposematic coloration.     

Avoidance of aposematic prey in European tits (Paridae): learned or innate?

Predators may either learn to avoid aposematic prey or may avoidit because of an innate bias. Learned as well as innate avoidancehas been observed in birds, but the existing evidence is basedon experiments with rather few unrelated model species. We comparedthe origin of avoidance in European species of tits (Paridae).First, we tested whether wild-caught birds (blue tits, greattits, crested tits, coal tits, willow tits, and marsh tits)avoid aposematic (red and black) adult firebugs Pyrrhocorisapterus (Heteroptera) more than nonaposematic (brown painted)ones. Larger proportion of birds avoided aposematic than brown-paintedfirebugs in majority of species (except coal tits). Second,we tested whether naive hand-reared birds of 4 species (bluetits, great tits, crested tits, and coal tits) attack or avoidaposematic and nonaposematic firebugs, both novel for them.Behavior of the naive blue tits and coal tits was similar tothat of the wild-caught birds; majority of them did not attackthe firebugs. Contrastingly, the naive great tits and crestedtits behaved differently than the wild-caught conspecific adults;majority of the wild-caught birds avoided the aposematic firebugs,whereas the naive birds usually did not show any initial avoidanceand had to learn to avoid the aposematic prey. Our results showthat the origin of avoidance may be different even in closelyrelated species. Because blue tits and coal tits avoided notonly aposematic firebugs but also their brown-painted form,we interpret their behavior as innate neophobia rather thaninnate bias against the warning coloration.     

Seasonal Abundance and Predatory Potential of <Emphasis Type="Italic">Stethorus aptus</Emphasis> Kapur (Coleoptera: Coccinellidae): A Biocontrol Agent of Tea Red Spider Mite <Emphasis Type="Italic">Oligonychus coffeae</Emphasis> Nietner (Acarina: Tetranychidae)

The tea red spider mite, Oligonychus coffeae Nietner is one of the major pests of tea plants in North-east India. The ladybird beetle, Stethorus aptus Kapur, is a newly reported predator of O. coffeae. Predatory efficiency study of S. aptus under laboratory conditions revealed that adult of S. aptus consumed significantly more mites than larvae. In free choice condition, the predator consumed within a range of 48–56 adults and 82–90 larvae of O. coffeae whereas the 3rd and 4th instar larvae of S. aptus consumed 20–26 adults and 50–60 larvae of O. coffeae per day respectively. Population dynamics of S. aptus was observed for 1 year under field conditions. The maximum density of the predator was recorded during January to March and it gradually declined from September onwards. Population of S. aptus showed positive correlation with its prey O. coffeae and relative humidity while effect of other factors was insignificant.     

Attacks by predators on artificial cryptic and aposematic insect larvae

Colour and colour patterns seem to be especially important visual warning signals for predators, which might have innate or learned ability to avoid aposematic prey. To test the importance of larval colour pattern of the aposematic ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), an invasive alien species in Europe, we presented the plasticine models of aposematic larvae to wild and naïve birds. We studied the attacks on aposematic larvae of various patterns and colours in nature and in an outdoor aviary. The larvae were cryptic (green), aposematic (resembling those of the H. axyridis larvae), and semi-aposematic (i.e., black but missing the typical orange patches of H. axyridis larvae). We detected attacks on 71 larvae out of 450 (i.e., 2.6% daily predation). Twenty-nine attacks were made by birds, 37 by arthropods, and five by gastropods. Wild birds attacked green and black larvae significantly more often than aposematic larvae. Colour did not have an effect on attacks by arthropods. The experiment with naïve birds was conducted in an outdoor aviary, where naïve great tits, Parus major L., were offered the same artificial larvae as in the first experiment. In total, 57 of 90 exposed larvae were attacked by birds (i.e., 28% daily predation), and green larvae were attacked significantly more than the aposematic larvae (but not more than black larvae). Our results imply that aposematic larvae of H. axyridis are more than 12× less likely to be predated by birds than green larvae in nature. The aposematic pattern represented a more effective signal than the semi-aposematic signal. The ability to reject aposematic prey seemed to be innate in our birds.     

Avian predators attack aposematic prey more forcefully when they are part of an aggregation

Defended insects often advertise their unprofitability to potential predators using conspicuous aposematic coloration. Many aposematic insects are also gregarious, and it has been suggested that the aggregation of defended prey may have facilitated the evolution of aposematic coloration. Empirical studies have demonstrated that birds are more wary of aggregated aposematic prey, and learn to avoid them more quickly than solitary prey. However, many aposematic insects survive being attacked by birds, and the effect of aggregation on post-attack survival has not previously been investigated. Using domestic chicks as predators and artificially manipulated mealworms as prey, we provide empirical evidence that predators attack aggregated aposematic prey more forcefully than solitary prey, reducing the likelihood of prey surviving an attack. Hence, we suggest that previous works concluding that aggregation was an important pre-requisite for the evolution of aposematism may have overestimated the fitness benefits of aggregation, since aggregated prey may be attacked less but are also less likely to survive an attack.     

Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey

Recently there has been debate over the importance of innateavoidance of aposematic prey by predators, particularly birds.There is evidence that the predators have innate or unlearned,thus, inherited avoidance against certain colors, but whetherthere is any innate avoidance against gregariousness or conspicuousnessis unclear. Previously predator behavior toward these charactersof aposematic prey have been tested in separate experiments.We designed an experiment to separate inheritance toward color,gregariousness, and conspiucuosness. We simultaneously offeredthe predators warningly colored and nonwarningly colored preyitems, both aggregated and solitary, on white (conspicuous)or brown (cryptic) backgrounds. The predators we used were naive (handraised), wild-caught yearling and adult great tits (Parus major L.).The results confirm previous results regarding the innate avoidanceof color. Naive predators seemed to have a genetically or culturallytransmitted avoidance of yellow and black prey compared to brownprey. Surprisingly, yearling wild-caught great tits were moreselective than adults, which did not show as strong avoidanceof yellow and black prey. More importantly, birds did not findgregarious prey more aversive than single prey, which indicatesthat grouping alone does not serve as an innate avoidance signal.Conspicuousness itself was not aversive to the predators. Ourresults suggest that the avoidance against a particular colorpattern probably has an inherited basis, whereas gregariousand conspicuous characters of prey presumably aid the avoidancelearning.     

How Do Predators Learn to Recognize a Mimetic Complex: Experiments with Naive Great Tits and Aposematic Heteroptera

We tested the importance of innate wariness, avoidance learning, memory and generalization for the formation of predatory behaviour in naive great tits (Parus major) towards mimetic complex of four aposematic species of true bugs (Insecta: Hemiptera: Heteroptera): Lygaeus equestris, Spilostethus saxatilis, Pyrrhocoris apterus and Graphosoma lineatum. The birds showed almost no innate wariness against the aposematically coloured bugs, although a hidden wariness elicited by defensive chemicals of some of the bug species is not excluded. Naive birds learned to avoid different species at different rates, which resulted in different prey mortalities. The avoidance learning was faster when the defensive chemicals produced an immediate irritating effect (particularly when squirted into distance – G. lineatum) than when they caused sickness several minutes after the consumption (P. apterus). The experience of birds from learning to avoid a particular species of bug affected their subsequent behaviour to other species – experience with better‐defended species resulted in longer attack latencies, more cautious attacks, broader generalization and lower prey mortality. The least defended species, P. apterus, benefited from the experience of birds with better‐defended species, whereas the birds' experience with P. apterus did not reduce mortality risk of the other species comparably. Judging from the inexperienced young birds, the mimetic relationships are likely to be quasi‐Batesian. However, as wild‐caught great tits avoid all the four species to the same extent, the relationships may become more mutualistic (quasi‐Müllerian) in later phases of learning under natural conditions. The relationships among species in the mimetic complex thus seem to depend on the amount of experience of the bird predators.     

Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars

1. Aposematism is a widely used antipredator strategy in which an organism possesses both warning coloration and unprofitable characters. Theoretical evidence suggests that aposematic colour should develop when high opportunity costs imposed by crypsis force an organism to engage in conspicuous behaviours. Hence, it is expected that ontogenetic colour change (OCC) in larval insects should include aposematism when foraging needs compel behavioural modifications that preclude a continued state of crypsis. 2. To test this idea, I first investigated whether OCC in caterpillars of the panic moth Saucrobotys futilalis was indicative of a switch from cryptic to aposematic coloration. I then examined the context of panic moth OCC as it related to foraging patterns and behavioural conspicuousness. 3. Early Saucrobotys instars are a cryptic green, but later instars become progressively more orange and develop black spots. Early instar larvae forage cryptically on the inner parenchyma of silked-together host plant leaves to avoid predation, but are rapidly forced to engage in conspicuous foraging behaviours as they outgrow the resources afforded by their shelters. Both coloration and behaviour reach maximal conspicuousness in final instar larvae. 4. As predicted, OCC encompassed a change from crypsis to aposematism in Saucrobotys. Aposematic function was demonstrated by changes in both antipredator behaviour patterns and effectiveness of predator deterrence in early and late instars. Moreover, increased opportunity costs of crypsis and behavioural conspicuousness coincided with the onset of aposematic coloration. 5. This pattern of OCC suggests that aposematic coloration in Saucrobotys develops as a response to constraints imposed by crypsis. Moreover, my study illustrates the importance of the study of ontogenetic patterns in determining how behaviour, morphology, and predator responses interact to influence the initial evolution of phenomena such as aposematism.