The interplay between multiple predators and prey colour divergence

Evolutionary divergence in the coloration of toxic prey is expected when geographic variation in predator composition and behavior favours shifts in prey conspicuousness. A fundamental prediction of predator‐driven colour divergence is that the local coloration should experience lower predation risk than novel prey phenotypes. The dorsal coloration of the granular poison frog varies gradually from populations of conspicuous bright red frogs to populations of dull green and relatively cryptic frogs. We conducted experiments with clay models in four populations to examine the geographic patterns of taxon‐specific predation. Birds avoided the local phenotype while lizards consistently selected for decreased conspicuousness and crab predation did not depend on frog coloration. Importantly, birds and lizards favoured low conspicuousness in populations where relatively cryptic green morphs have evolved. This study provides evidence for the interplay among distinct selective pressures, from multiple‐predator taxa, acting on the divergence in protective coloration of prey species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 580–589.     

You can run--or you can hide: optimal strategies for cryptic prey against pursuit predators

We consider the optimal behavior of a cryptic prey individualas it is approached by a predator searching for prey. Althoughthe predator has not yet discovered the prey, it has an increasinglikelihood of doing so as it gets closer to the prey. Further,the closer the predator is to the prey when it discovers it,the more likely the predator will be to capture the prey. Thesearguments suggest that the prey should flee before the predatordiscovers it. However, the act of fleeing will alert the predatorto the presence of the prey and trigger an attack that mightnot have occurred otherwise. We capture these conflicting outcomesin a mathematical model, which we then use to predict the optimalbehavior of the prey and predator. We argue that the optimalstrategy for the prey is either to run as soon as they detecta predator approaching or to only flee in response to havingbeen detected by the predator. Running as soon as the predatoris detected is associated with low predator search speeds, alow nonpredation cost to running, a large advantage to the preyin initiating chases rather than reacting, limited ability tospot the predator at distance, a high ability to spot prey bythe predator, and a high probability that chases will be successful.The optimal strategy for the predator depends on whether itscurrent trajectory is taking it closer to or further from theprey. In the latter case, the predator should attack immediatelyon discovering the prey; in the former case, it should delayits attack until it reaches the point on its current trajectorywhere distance to the prey is minimized.     

Better the devil you know: avian predators find variation in prey toxicity aversive

Toxic prey that signal their defences to predators using conspicuous warning signals are called ‘aposematic’. Predators learn about the toxic content of aposematic prey and reduce their attacks on them. However, through regulating their toxin intake, predators will include aposematic prey in their diets when the benefits of gaining the nutrients they contain outweigh the costs of ingesting the prey''s toxins. Predators face a problem when managing their toxin intake: prey sharing the same warning signal often vary in their toxicities. Given that predators should avoid uncertainty when managing their toxin intake, we tested whether European starlings (Sturnus vulgaris) preferred to eat fixed-defence prey (where all prey contained a 2% quinine solution) to mixed-defence prey (where half the prey contained a 4% quinine solution and the other half contained only water). Our results support the idea that predators should be more ‘risk-averse’ when foraging on variably defended prey and suggest that variation in toxicity levels could be a form of defence.     

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.     

Costs and benefits of defences induced by predators differing in dangerousness

While theoretical studies predict that inducible defences should be fine-tuned according to the qualities of the predator, very few studies have investigated how dangerousness of predators, i.e. the rate at which predators kill prey individuals, affects the strength of phenotypic responses and resulting benefits and costs of induced defences. We performed a comprehensive study on fitness consequences of predator-induced responses by involving four predators (leech, water scorpion, dragonfly larva and newt), evaluating costs and benefits of responses, testing differences in dangerousness between predators and measuring responses in several life history traits of prey. We raised Rana dalmatina tadpoles in the presence of free-ranging predators, in the presence of caged predators, and exposed naive and experienced tadpoles to free-ranging predators. Tadpoles adjusted the intensities of their behavioural and morphological defences to predator dangerousness. Survival was lower in the nonlethal presence of the most dangerous predator, while we could not detect costs of induced defences at or after metamorphosis. When exposed to free-ranging predators, small, but not large, tadpoles benefited from exhibiting an induced phenotype in terms of elevated survival when compared to naive tadpoles, but we did not observe higher survival either in tadpoles exhibiting more extreme phenotypes or in tadpoles exposed to the type of predator they were raised with. These results indicate that while predator-induced defences can mirror dangerousness of predators, costs and benefits do not necessarily scale to the magnitude of plastic responses.     

Inducible defences in Daphnia depend on latent alarm signals from conspecific prey activated in predators

Some water fleas (Daphnia spp.) undergo phenotypic changes when exposed to chemical signals from predators. The chemical signals have been assumed to be of predator origin (i.e. kairomones), since juices of crushed Daphnia have been found ineffective. We speculated that latent alarm signals could be present in Daphnia, to be activated in predators following ingestion. Accordingly, fish predators were fed earthworms for 10 weeks to remove Daphnia remains from their gastro-intestinal tracts. Following another 6 days of earthworm feeding, water conditioned by fish induced no morphological changes in D. galeata. When fish were alternatively fed Daphnia for 6 days, changes were induced with fish-conditioned water. Extracts made from intestines of earthworm-fed fish, homogenized with earthworms, gave no morphological changes, but intestines of the same origin homogenized with Daphnia did. Similar results were found when earthworms and Daphnia were homogenized with fish liver. Freshly frozen extracts of homogenized Daphnia gave no detectable changes at first instar stage in test animals, whereas extracts of Daphnia that had been kept at room temperature did induce such changes. Our results suggest that Daphnia respond to latent conspecific alarm signals (i.e. 'dormant' pheromones) that are activated by intestinal or bacterial enzymes in predators or in the water.     

Targeted predation of extrafloral nectaries by insects despite localized chemical defences

Extrafloral (EF) nectaries recruit carnivorous arthropods that protect plants from herbivory, but they can also be exploited by nectar thieves. We studied the opportunistic, targeted predation (and destruction) of EF nectaries by insects, and the localized chemical defences that plants presumably use to minimize this effect. In field and laboratory experiments, we identified insects that were possibly responsible for EF nectary predation in Vicia faba (fava bean) and determined the extent and accuracy of the feeding damage done to the EF nectaries by these insects. We also performed biochemical analyses of plant tissue samples in order to detect microscale distribution patterns of chemical defences in the area of the EF nectary. We observed selective, targeted feeding on EF nectaries by several insect species, including some that are otherwise not primarily herbivorous. Biochemical analyses revealed high concentrations of l-3,4-dihydroxyphenylalanine, a non-protein amino acid that is toxic to insects, near and within the EF nectaries. These results suggest that plants allocate defences to the protection of EF nectaries from predation, consistent with expectations of optimal defence theory, and that this may not be entirely effective, as insects limit their exposure to these defences by consuming only the secreting tissue of the nectary.     

Escape behaviour and ultimate causes of specific induced defences in an anuran tadpole

Induced defences, such as the predator avoidance morphologies in amphibians, result from spatial or temporal variability in predation risk. One important component of this variability should be the difference in hunting strategies between predators. However, little is known about how specific and effective induced defences are to different types of predators. We analysed the impact of both pursuing (fish, Gasterosteus aculeatus) and sit-and-wait (dragonfly, Aeshna cyanea) predators on tadpole (Rana dalmatina) morphology and performance (viz locomotive performance and growth rate). We also investigated the potential benefits of the predator-induced phenotype in the presence of fish predators. Both predators induced deeper tail fins in tadpoles exposed to threat of predation, and stickleback presence also induced longer tails and deeper tail muscles. Morphological and behavioural differences resulted in better escape ability of stickleback-induced tadpoles, leading to improved survival in the face of stickleback predation. These results clearly indicate that specific morphological responses to different types of predators have evolved in R. dalmatina. The specific morphologies suggest low correlations between the traits involved in the defence. Independence of traits allows prey species to fine-tune their response according to current predation risk, so that the benefit of the defence can be maximal.     

Birds exploit herbivore‐induced plant volatiles to locate herbivorous prey

Arthropod herbivory induces plant volatiles that can be used by natural enemies of the herbivores to find their prey. This has been studied mainly for arthropods that prey upon or parasitise herbivorous arthropods but rarely for insectivorous birds, one of the main groups of predators of herbivorous insects such as lepidopteran larvae. Here, we show that great tits (Parus major) discriminate between caterpillar‐infested and uninfested trees. Birds were attracted to infested trees, even when they could not see the larvae or their feeding damage. We furthermore show that infested and uninfested trees differ in volatile emissions and visual characteristics. Finally, we show, for the first time, that birds smell which tree is infested with their prey based on differences in volatile profiles emitted by infested and uninfested trees. Volatiles emitted by plants in response to herbivory by lepidopteran larvae thus not only attract predatory insects but also vertebrate predators.     

Reciprocal phenotypic plasticity in a predator–prey system: inducible offences against inducible defences?

We describe one of the first examples of reciprocal phenotypic plasticity in a predator–prey system: the interaction between an inducible defence and an inducible offence. When confronted with the predatory ciliate Lembadion bullinum, the hypotrichous ciliate Euplotes octocarinatus develops protective lateral wings, which inhibit ingestion by the predator. We show that L. bullinum reacts to this inducible defence by expressing an inducible offence – a plastic increase in cell size and gape size. This counteraction reduced the effect of the defence, but did not completely neutralize it. Therefore, the defence remained beneficial for E. octocarinatus. From L. bullinum's point of view, the increase in feeding rate because of the offence was not larger than the increase in mean cell volume and apparently, did not increase the predator's fitness. Therefore, the inducible offence of L. bullinum does not seem to be an effective counter‐adaptation to the inducible defence of E. octocarinatus.     

Active foraging for toxic prey during gestation in a snake with maternal provisioning of sequestered chemical defences

Many animals sequester dietary defensive compounds and incorporate them into the offspring, which protects the young against predation. One possible but poorly investigated question is whether females of such species actively prey upon toxic diets. The snake Rhabdophis tigrinus sequesters defensive steroids from toads consumed as prey; it also feeds on other amphibians. Females produce chemically armed offspring in direct proportion to their own level of toad-derived toxins by provisioning the toxins to their eggs. Our field observations of movements and stomach contents of radio-tracked R. tigrinus showed that gravid snakes preyed upon toads by actively foraging in the habitat of toads, even though toads were a scarce resource and toad-searching may incur potential costs. Our Y-maze experiments demonstrated that gravid females were more likely to trail the chemical cues of toads than were males or non-gravid females. These results showed behavioural switching in females and active foraging for scarce, toxic prey during gestation. Because exploitation of toads by gravid females results in their offspring being more richly endowed with prey-derived toxins, active foraging for toxic prey is expected to be an adaptive antipredator trait, which may enhance chemical defence in offspring.     

Masquerading predators deceive prey by aggressively mimicking bird droppings in a crab spider

In aggressive mimicry, a predator accesses prey by mimicking the appearance and/or behavior of a harmless or beneficial model in order to avoid being correctly identified by its prey. The crab spider genus Phrynarachne is often cited as a textbook example of masquerading as bird droppings (BDs) in order to avoid predation. However, Phrynarachne spiders may also aggressively mimic BDs in order to deceive potential prey. To date, there is no experimental evidence to support aggressive mimicry in masquerading crab spiders; therefore, we performed a field survey, a manipulative field experiment, and visual modeling to test this hypothesis using Phrynarachne ceylonica. We compared prey-attraction rates among BDs, spiders, and control empty leaves in the field. We found that although all prey combined and agromyzid dipterans, in particular, were attracted to BDs at a higher rate than to spiders, other dipterans and hymenopterans were attracted to BDs at a similar rate as to spiders. Both spiders and BDs attracted insects at a significantly higher rate than did control leaves. As predicted, prey was attracted to experimentally blackened or whitened spiders significantly less frequently than to unmanipulated spiders. Finally, visual modeling suggested that spiders and BDs can be detected by dipterans and hymenopterans against background leaves, but they are indistinguishable from each other. Taken together, our results suggest that insects lured by spiders may misidentify them as BDs, and bird-dropping masquerading may serve as aggressive mimicry in addition to predator avoidance in P. ceylonica.     

Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula

Direct and indirect defences against feeding induced by chewing (Spodoptera littoralis) and piercing-sucking (Tetranychus urticae) herbivores, as well as components of signal transduction, were investigated in the model legume Medicago truncatula. Emitted volatiles, representing a mechanism of indirect defence, were measured and identified by gas chromatography/mass spectrometry (GC-MS). As elements of direct defence, the accumulation of phenolic compounds and of reactive oxygen species (ROS) was assessed using microscopic techniques. Jasmonic acid (JA) and salicylic acid (SA) concentrations were assessed as putative components of signal transduction. Volatile profiles revealed a sizeable number of different substances emitted, particularly sesquiterpenoids. The qualitative composition clearly differed depending on the type of herbivory. The same held true for JA and SA concentrations. Also, deposition of phenolic compounds and the production of ROS around the wounding sites could be detected. Conspicuous differences were found in indirect defence and signalling for different types of herbivory. In contrast, no divergence in direct defences was observed; furthermore, the traits investigated exhibited striking similarities to reactions known to occur upon pathogen attack.     

Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera)

Persistent questions concerning the warning coloration of unpalatable insects address whether the bright aposematic colour itself or its combination with a species-specific dark pattern is the key factor in their protection against insectivorous birds, and how chromatic polymorphism originates and is maintained in aposematics. In the present study, these questions were tested experimentally, using the birds Parus major , Parus caeruleus , Erithacus rubecula , and Sylvia atricapilla as predators, and chromatically polymorphic firebug Pyrrhocoris apterus : red wild form, white, yellow, and orange mutants (all four of them with the same black melanin pattern, the mutants differing in colour of pteridine pigments only) and the nonaposematic brown-painted wild form as prey. The results show that a specific colour is essential for the birds to recognize the specific aposematic prey; the melanin pattern is not sufficient. White mutants were no better protected than nonaposematic firebugs; red wild-type and orange mutants were equally well protected against all bird species; and the reaction of birds to yellow mutants was species-specific. An evolutionary scenario of 'recurrent recessive mutations' is formulated to explain the origin of colour polymorphism in some aposematics.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 143–153.     

Phenotypic variability can promote the evolution of adaptive plasticity by reducing the stringency of natural selection

Adaptive phenotypic plasticity is a potent but not ubiquitous solution to environmental heterogeneity, driving interest in what factors promote and limit its evolution. Here, a novel computational model representing stochastic information flow in development is used to explore evolution from a constitutive phenotype to an adaptively plastic response. Results show that populations tend to evolve robustness to developmental stochasticity, but that this evolved robustness limits evolvability; specifically, robust genotypes have less ability to evolve adaptive plasticity when presented with a mix of both the ancestral environment and a new environment. Analytic calculations and computational experiments confirm that this constraint occurs when the initial mutational steps towards plasticity are pleiotropic, such that mutant fitnesses decline in the environment to which their parents are well‐adapted. Greater phenotypic variability improves evolvability in the model by lessening this decline as well as by improving the fitness of partial adaptations to the new environment. By making initial plastic mutations more palatable to natural selection, phenotypic variability can increase the evolvability of an innovative, plastic response without improving evolvability to simpler challenges such as a shifted optimum in a single environment. Populations that evolved robustness by negative feedback between the trait and its rate of change show a particularly strong constraining effect on the evolvability of plasticity, revealing another mechanism by which evolutionary history can limit later innovation. These results document a novel mechanism by which weakening selection could actually stimulate the evolution of a major innovation.     

Novel evidence for systemic induction of silicon defences in cucumber following attack by a global insect herbivore

1. Silicon (Si) is a beneficial nutrient that has been reported to ameliorate many abiotic and biotic stresses in plants, including insect herbivory. Insect herbivory has been shown to induce Si defences in plants, although the magnitude and nature of induction remain largely ambiguous. In particular, it is unclear whether herbivore induction of Si defences is confined to attacked tissues (local) or occurs elsewhere in the plant (systemic). 2. We grew cucumber, Cucumis sativus L. plants (var. Burpless F1 and Beit Alpha), an intermediate Si accumulator, hydroponically under Si-supplemented or Si-free conditions and measured the level of Si induction caused by a polyphagous chewing insect, the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). We also examined the impacts of Si on insect performance by conducting in vitro feeding assays on excised leaves (ex situ) and intact leaves on plants (in situ). 3. Herbivory significantly increased Si accumulation both locally in attacked leaves (21% increase in Beit Alpha and 17% in Burpless F1) and systemically in non-attacked leaves (19% increase in Beit Alpha and 10% in Burpless F1). Si supplementation significantly increased % foliar Si and C:N ratio, while significantly decreasing larval relative consumption (RC) and relative growth rate (RGR) in the in situ assays. In ex situ assays, however, Si only reduced larval RGR when fed on Beit Alpha plants. 4. Our results confirm that Si-based defences can also operate in moderate Si-accumulating plants and, for the first time, that insect herbivory induces systemic Si accumulation equivalently between plant varieties.