Frequency-dependent predation, crypsis and aposematic coloration

Frequency-dependent predation may maintain or prevent colour pattern polymorphisms in prey, and can be caused by a variety of biological phenomena, including perceptual processes (search images), optimal foraging and learning. Most species are preyed upon by more than one predator species, which are likely to differ in foraging styles, perceptual and learning abilities. Depending upon the interaction between predator vision, background and colour pattern parameters, certain morphs may be actively maintained in some conditions and not in others, even with the same predators. More than one kind of predator will also affect stability, and only slight changes in conditions can cause a transition between polymorphism and monomorphism. Frequency-dependent selection is not a panacea for the explanation of variation in animal colour patterns, although it may be important in some systems.     

Increased predation of nutrient-enriched aposematic prey

Avian predators readily learn to associate the warning coloration of aposematic prey with the toxic effects of ingesting them, but they do not necessarily exclude aposematic prey from their diets. By eating aposematic prey ‘educated’ predators are thought to be trading-off the benefits of gaining nutrients with the costs of eating toxins. However, while we know that the toxin content of aposematic prey affects the foraging decisions made by avian predators, the extent to which the nutritional content of toxic prey affects predators'' decisions to eat them remains to be tested. Here, we show that European starlings (Sturnus vulgaris) increase their intake of a toxic prey type when the nutritional content is artificially increased, and decrease their intake when nutritional enrichment is ceased. This clearly demonstrates that birds can detect the nutritional content of toxic prey by post-ingestive feedback, and use this information in their foraging decisions, raising new perspectives on the evolution of prey defences. Nutritional differences between individuals could result in equally toxic prey being unequally predated, and might explain why some species undergo ontogenetic shifts in defence strategies. Furthermore, the nutritional value of prey will likely have a significant impact on the evolutionary dynamics of mimicry systems.     

Frequency-dependent selection on aposematic prey: some experiments

Experiments to measure the strength of frequency-dependent selection on dimorphic populations of distasteful, brightly coloured prey were carried out, using pastry cylinders as prey and wild birds as predators. When the two forms were haphazardly intermingled, the birds took a relative excess of whichever form happened to be the rarer if all prey in the population were distasteful but selected the forms independently of frequency if they were all neutral in flavour. They did not take an excess of the rarer form from populations of distasteful prey when that form was distributed in a single clump rather than evenly dispersed among the commoner form. This confirms the expectation that rarer forms of aposematic animals are at a frequency-dependent disadvantage when they are intermingled with commoner forms but not when they occur in clusters.     

Avian predators taste-reject aposematic prey on the basis of their chemical defence

Avian predators learn to avoid defended insects on the basis of their conspicuous warning coloration. In many aposematic species, the level of chemical defence varies, with some individuals being more defended than others. Sequestration and production of defence chemicals is often costly and therefore less defended individuals enjoy the benefits of the warning signal without paying the full costs of chemical production. This is a fundamental theoretical problem for the evolutionary stability of aposematism, since less defended individuals appear to be at a selective advantage. However, if predators sample aposematic prey and selectively reject individuals on the basis of their chemical investment, aposematism could become evolutionarily stable. Previous research aimed at testing whether birds can use taste to discriminate between palatable and unpalatable prey has been confounded by other experimental factors. Here, we show that birds can taste and reject prey entirely on the basis of an individual's level of chemical defence and more importantly, they can make decisions on whether or not to consume a defended individual based upon their level of chemical investment. We discuss these results in relation to the evolution of aposematism, mimicry and defence chemistry.     

Frequency-dependent predation and maintenance of prey polymorphism

In positive frequency-dependent predation, predation risk of an individual prey correlates positively with the frequency of that prey type. In a number of small-scale experiments individual predators have shown frequency-dependent behaviour, often leading to the conclusion that a population of such predators could maintain prey polymorphism. Using simulations, I studied the dynamics of frequency-dependent predation and prey polymorphism. The model suggests that persistence of prey polymorphism decreases with increasing number of predators that show frequency-dependent behaviour, questioning conclusions about polymorphism based on experiments with few predators. In addition, prey population size, prey crypsis, difference in crypsis between prey morphs and the way the behaviour was adjusted affected the persistence of polymorphism. Under some circumstances prey population remained polymorphic for a shorter time under frequency-dependent than under frequency-independent predation. This suggests that although positive frequency-dependent predator behaviour may maintain prey polymorphism, it is not a sufficient condition for persistent prey polymorphism.     

Intense or spatially heterogeneous predation can select against prey dispersal

Dispersal theory generally predicts kin competition, inbreeding, and temporal variation in habitat quality should select for dispersal, whereas spatial variation in habitat quality should select against dispersal. The effect of predation on the evolution of dispersal is currently not well-known: because predation can be variable in both space and time, it is not clear whether or when predation will promote dispersal within prey. Moreover, the evolution of prey dispersal affects strongly the encounter rate of predator and prey individuals, which greatly determines the ecological dynamics, and in turn changes the selection pressures for prey dispersal, in an eco-evolutionary feedback loop. When taken all together the effect of predation on prey dispersal is rather difficult to predict. We analyze a spatially explicit, individual-based predator-prey model and its mathematical approximation to investigate the evolution of prey dispersal. Competition and predation depend on local, rather than landscape-scale densities, and the spatial pattern of predation corresponds well to that of predators using restricted home ranges (e.g. central-place foragers). Analyses show the balance between the level of competition and predation pressure an individual is expected to experience determines whether prey should disperse or stay close to their parents and siblings, and more predation selects for less prey dispersal. Predators with smaller home ranges also select for less prey dispersal; more prey dispersal is favoured if predators have large home ranges, are very mobile, and/or are evenly distributed across the landscape.     

Shorebird predation may cause discrete generations in an amphipod prey

We examine the possible impact of intense, periodic predation by the semipalmated sandpiper Calidris pusilla, on the life history patterns of its amphipod prey, Co-rophium volutator We compare populations from two mudflats, one of which is visited by shorebirds on their annual migration south, and one which physically appears very similar but is not visited by the birds The Corophium population exposed to intense predation had two distinct peaks in density within the season, corresponding to two generations, and the two cohorts had constrained size distributions, and relatively synchronized timing of reproduction On the mudflat not visited by sandpipers, densities increased m spring and then remained constant through summer Reproduction was continuous The mid-summer decline in amphipod density on the mudflat used by sandpipers could not be attributed directly to sandpiper predation as had been previously argued We interpret the decline as the result of a synchronized natural die-off after reproduction Selective predation on large amphipods may contribute to the second peak in density by increasing juvenile survivorship due to the removal of competing adults Size-selective predation by sandpipers causes the overwintering cohort to have a restricted size range m the autumn, and this synchrony persists through to the reproductive period of the following spring We do not exclude the possibility that these differences in life history have been influenced in an evolutionary sense by the long history of intense periodic predation     

Protean defence by prey animals

Summary Attention is drawn to the widespread occurrence ofprotean phenomena, in which the appearance and behaviour of prey animals are rendered variable and irregular, as a weapon in the biological arms race between predators and their prey. Protean behaviour is defined as that behaviour which is sufficiently unsystematic to prevent a reactor predicting in detail the position or actions of the actor.Single prey animals frequently flee from a predator in an irregular manner, zigzagging, spinning, looping, or bouncing. Thissingle erratic display occurs widely in the Animal Kingdom, and may also be utilised in everyday movements of potential prey as insurance against possible attack. Examples are given.In a group of prey animals the protean aspect of escape is enhanced by the effect of numbers. In scatter reactions the effect is of multiple choice and of the simultaneous operation of several single erratics. In mobbing displays there are also successive changes in the actors' behavioural role. In protean deterrence the shuffling of individuals within a tightly packed group prevents a predator from singling one out for attack.In many species the confusing effect of changes in movement and behavioural role is enhanced by rapid changes in appearance, particularly colour.It is suggested that those prey individuals which employ escape patterns unfamiliar to the predator will tend to be at a selective advantage. During phylogeny this is likely to lead to intra-specific and inter-specific increase in the number and diversity of escape behaviours. Apostatic polymorphism is seen as a special case of protean variation within populations.There is evidence that protean displays operate by arousing neurological conflict, thereby delaying the predator's reactions and reducing the effectiveness of predatory mechanisms. Also they insure against learned countermeasures by incorporating irregularities as a basic principle. It is stressed that the irregular variability of protean displays is not accidental but has been selected for in phylogeny. A number of poorly understood behavioural aspects of the ecology of predator-prey relationships are thus united in a single theory.     

Flooding regimes increase avian predation on wildlife prey in tidal marsh ecosystems

Within isolated and fragmented populations, species interactions such as predation can cause shifts in community structure and demographics in tidal marsh ecosystems. It is critical to incorporate species interactions into our understanding when evaluating the effects of sea‐level rise and storm surges on tidal marshes. In this study, we hypothesize that avian predators will increase their presence and hunting activities during high tides when increased inundation makes their prey more vulnerable. We present evidence that there is a relationship between tidal inundation depth and time of day on the presence, abundance, and behavior of avian predators. We introduce predation pressure as a combined probability of predator presence related to water level. Focal surveys were conducted at four tidal marshes in the San Francisco Bay, California where tidal inundation patterns were monitored across 6 months of the winter. Sixteen avian predator species were observed. During high tide at Tolay Slough marsh, ardeids had a 29‐fold increase in capture attempts and 4 times greater apparent success rate compared with low tide. Significantly fewer raptors and ardeids were found on low tides than on high tides across all sites. There were more raptors in December and January and more ardeids in January than in other months. Ardeids were more prevalent in the morning, while raptors did not exhibit a significant response to time of day. Modeling results showed that raptors had a unimodal response to water level with a peak at 0.5 m over the marsh platform, while ardeids had an increasing response with water level. We found that predation pressure is related to flooding of the marsh surface, and short‐term increases in sea levels from high astronomical tides, sea‐level rise, and storm surges increase vulnerability of tidal marsh wildlife.     

Benefit by contrast: an experiment with live aposematic prey

Aposematic prey often have a coloration that contrasts withthe background. One beneficial effect of such conspicuous colorationis that it produces faster and more durable avoidance by predators.Another suggested benefit is that prey that contrast with thebackground are more quickly discerned and recognized as unpalatableby experienced predators. To further investigate the effectsof prey contrast on predator behavior, I conducted an experimentwith young chicks (Gallus gallus domesticus) as predators onlive aposematic and nonaposematic prey. Birds with prior experienceof both prey types were allowed into an arena with both palatableprey and aposematic prey on backgrounds that either closelymatched or contrasted with the coloration of the aposematicprey. Also, the time a bird had available to decide to attacka prey was manipulated by including a competing chick or not.The experienced birds showed greater attack latencies for aposematicprey on more contrasting backgrounds, and aposematic prey werealso attacked to a greater extent when on a matching background.The presence of a competitor generated similar effects, wherebirds in high competition attacked more and faster comparedto birds subjected to lower degree of competition, but therewas no interaction between competition and contrast. Thus,the experiment provides evidence that prey contrast againstthe background may produce better recognition and avoidance,independently of predator viewing time.     

Frequency-dependent predation by birds at edges and interiors of woodland

Structural variations between edge and interior areas within forest fragments may bring about differences in food availability that may influence the selective behaviour of predators and prey population dynamics. The purpose of this paper was to assess patterns of artificial prey selection by wild birds (House Sparrow Passer domesticus and Rock Dove Columba livid) between edge and interior areas of woodland, taking into account differences in prey frequency (10% of one food type and 90% of the other) and density (30 baits/m^-2 and 50 baits/m-²). Experiments were conducted at 24 plots in 3 forest fragments in the city of Madrid, Spain. Selectivity did not vary among parks or between densities. However, selectivity did vary with the frequency and location of baits, showing an anti-apostatic trend (baits were preferred at low rather than at high frequencies) that was more pronounced at interiors than at edges. Two possible factors that may account for stronger anti-apostatic selection at edges are the higher densities of predators and pedestrians found there. However, there are many other possible explanations, and no specific conclusion can be supported with the current data. The results of this study also point out that site heterogeneity should be taken into account in the experimental design of future studies on frequency-dependent food selection by wild birds, particularly in fragmented landscapes.     

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.     

Effects of novelty and gregariousness in survival of aposematic prey

We examined the reactions of captive wild great tits to novelunpalatable prey with (1) a traditional aposematic signal (blackand yellow) (2) a novel signal (light pink), and (3) a controlsignal (brown). Prey were offered either singly or in groupsto see whether novel signals with fewer possibilities for synergisticbenefits are more dependent on grouping than are the traditionalsignals. Indeed, responses of birds toward unpalatable preydepended significantly on spatial distribution of prey (groupingversus solitary) and the type of the signal. Birds avoided morethe traditional black and yellow signals than novel pink signalsin both experimental set ups, but both of these prey items survivedbetter in aggregation than solitarily. The success of traditionalsignals may demonstrate the importance of synergistic selectionacross species in the evolution of warning coloration (i.e.,Müllerian mimicry). Unpalatable prey individuals benefitstrongly from using similar color patterns. Our results suggestthat aggregation may be important for the evolution of novelsignals in particular, even if a synergistic selection componentis also present     

Birds learn to avoid aposematic prey by using the appearance of host plants

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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.     

The price of safety: food deprivation in early life influences the efficacy of chemical defence in an aposematic moth

Aposematism is the combination of a primary signal with a secondary defence that predators must learn to associate with one another. However, variation in the level of defence, both within and between species, is very common. As secondary defences influence individual fitness, this variation in quality and quantity requires an evolutionary explanation, particularly as it may or may not correlate with variation in primary signals. The costs of defence production are expected to play a considerable role in generating this variation, yet studies of the cost of chemical defence have focused on species that sequester their defences, while studies in species that produce them de novo are scarce. Here we examine effects of resource availability on the production of chemical defences in female wood tiger moths Arctia plantaginis. This species produces defensive fluids when attacked, and advertises this protection with bright colours on its hindwings. Furthermore, the chemicals in these fluids are produced de novo. In order to establish if the production of this chemical protection is costly, and thus resource‐limited, we manipulated resource availability (i.e. food) during larval development and measured its subsequent effects on adult chemical defence. We presented defensive fluids from female moths to wild blue tits, in the absence of any visual cues, to determine their effectiveness against avian predators. Our results demonstrate that the defensive fluids produced by female moths repel birds, and that these defences require resource investment to produce. We found that moths that were resource‐limited during development had less effective chemical defences, despite producing the same volume of defensive fluids as the control moths. As a reduction in available resources negatively influences the effectiveness of the chemical defence, resource availability may explain the variation seen among individuals.     

Site selection under differential predation risks by drifting prey in streams

We derived a model to predict site selection by drifting prey in streams. This model considers the conflicting demands between feeding and avoiding both benthic and drift predators. Our analysis suggests a ranking of site qualities based on the ratio of food acquisition rate to benthic predation risk (termed site value). Drifting organisms should accept a given site type when its site value exceeds the expected value of drifting, which is the average site value prey are likely to encounter adjusted for the costs of drifting. These costs are represented as drift predation risk and time that is lost from foraging as prey search for a better site. We contend that prey should rank site types in descending order based on site value and sequentially add site types to the acceptable category in order of highest rank until the addition of the next lowest ranked site decreases rather than increases the expected value of drifting. The best sites should be those with high food availability and low benthic predation risk. Prey should reject a site when drift predation risk is low, the proportion of acceptable site types is high, and the rate that prey settle from the drift is high. Interestingly, prey with the greatest locomotory ability should have the greatest propensity to drift because these individuals spend less time drifting, making them less susceptible to drift predators. Our model provides a framework to simultaneously integrate the effects of food availability, benthic predation risk, and drift predation risk on site selection of actively drifting prey.     

Evolutionary implications of the form of predator generalization for aposematic signals and mimicry in prey

Generalization is at the heart of many aspects of behavioral ecology; for foragers it can be seen as an essential feature of learning about potential prey, because natural populations of prey are unlikely to be perfectly homogenous. Aposematic signals are considered to aid predators in learning to avoid a class of defended prey. Predators do this by generalizing between the appearance of prey they have previously sampled and the appearance of prey they subsequently encounter. Mimicry arises when such generalization occurs between individuals of different species. Our aim here is to explore whether the specific shape of the generalization curve can be expected to be important for theoretical predictions relating to the evolution of aposematism and mimicry. We do this by a reanalysis and development of the models provided in two recent papers. We argue that the shape of the generalization curve, in combination with the nature of genetic and phenotypic variation in prey traits, can have evolutionary significance under certain delineated circumstances. We also demonstrate that the process of gradual evolution of Müllerian mimicry proposed by Fisher is particularly efficient in populations with a rich supply of standing genetic variation in mimetic traits.