Fast movement of densely aggregated prey increases the strength of anti-apostatic selection by wild birds

'Anti-apostatic' selection occurs when predators preferentially remove rare forms of prey, and has been demonstrated in both static (artificial) prey and moving (natural) prey. We performed 24 experiments at separate sites to test the effect of prey mobility on the strength of anti-apostatic selection by wild passerine birds. The prey were yellow and red Calliphora maggots and were presented in 9: 1 and 1: 9 ratios on a specially designed bird table. The temperature of the maggots, and hence their speed of movement, was adjusted by a combination of the ambient temperature and a candle under the bird table. Selection was anti-apostatic at all three classes of temperature and was strongest at the highest. We conclude that anti-apostatic selection on static prey is enhanced when they are made to move–possibly because the 'confusion effect' caused by the moving prey makes the birds concentrate more strongly on the rarer colours.     

Selection by wild birds on artificial dimorphic prey on varied backgrounds

Our aim was to test the effects of prey frequency and background composition on selection by free-ranging birds. We did three series of experiments with populations of grey and orange pastry prey scattered among coloured stones that made the prey either conspicuous or inconspicuous. Series 1 tested whether the predicted equilibrium frequency of the two prey types was influenced by the frequency of matching grey and orange stones. Birds at a single site were given a random sequence of combinations of prey frequency and stone frequency. Selection was dependent on background and the effect of prey frequency also varied with background. In series 2, we explored the frequency-independent effect of background: birds at five sites were given equal numbers of the two prey in three frequencies of matching stones and two of non-matching. There was a higher risk of predation for prey that matched rarer stones. In series 3 we attempted to measure, at a single site, the actual equilibrium prey frequencies in three different backgrounds: two extreme stone frequencies and one intermediate. Each experiment started with a population of equal numbers of grey and orange prey. After half the prey had been eaten we calculated the frequencies of the survivors and presented a new population of the original size but with the new prey frequencies; each experiment ran for 25 such 'generations'. The results suggested that at equilibrium the commoner 'morph' was the one that resembled the commoner colour of stone. Overall, our findings support the idea that visual selection can result in morph frequencies becoming related to the proportions of their matching background components and that this equilibrium will 'track' temporal or spatial changes in the background.     

Wild birds prefer the familiar of striped and unstriped artificial prey

Previous work has shown that wild birds can become trained to search for a prey type on the basis of its colour. The experiments presented in this paper extended this work to two types of green artificial prey that were identical except for the presence or absence of a red stripe. Wild birds at six widely separated sites were trained on populations of one type and then were offered a choice between equal numbers of the familiar type and a second type. All the populations were presented on lawn backgrounds. The experiments were then repeated at each site with the birds being trained on the second prey type. The results showed that there was a consistent tendency for the familiar prey type to be overpredated and this was statistically significant. The behaviour described in this paper, if it occurs in nature, could lead to frequency-dependent (apostatic) selection and the maintenance of polymorphism in prey species in which the morphs are distinguished by colour patterns.     

Can the dietary conservatism of predators compensate for positive frequency dependent selection against rare,conspicuous prey?

The evolution of conspicuous colouration in prey is puzzling because such coloration attracts the attention of predators. Anti-apostatic selection, in which rare prey forms are predated disproportionately often, is a second potential obstacle to the evolution of conspicuous colouration in prey, as bright novel prey forms are likely to be very rare when they first appear in populations. It has recently been postulated that dietary conservatism in predators, an extended feeding avoidance of novel prey, would allow novel conspicuous prey to survive and multiply despite anti-apostatic and conspicuousness effects. We tested this hypothesis for a novel prey type arising in an otherwise cryptic population, providing a direct test of whether anti-apostatic selection or the predators’ wariness to attack the novel prey type is the more important force acting on the novel conspicuous prey. We conducted our experiment in the “Novel World”; an experimental system designed to test predators’ foraging decisions in a large landscape. We found that the conspicuous, novel prey suffered high initial costs of conspicuousness compared with cryptic prey, since most of these prey were attacked during the first “generation”, with no opportunity to “reproduce”. However, a subset of the 17 birds (24%) were following a dietary conservative foraging strategy and they were reluctant to eat the novel prey. Interestingly these birds were not more neophobic or less explorative. Our data demonstrate how difficult it is for the novel conspicuous prey to survive in cryptic populations, but they also highlight the importance of the predator’s foraging strategies in helping to promote the evolution and maintenance of aposematism.     

The evolution of a Müllerian mimic in a spatially distributed community

Strong positive density-dependence should lead to a loss of diversity, but warning-colour and Müllerian mimicry systems show extraordinary levels of diversity. Here, we propose an analytical model to explore the dynamics of two forms of a Müllerian mimic in a heterogeneous environment with two alternative model species. Two connected populations of a dimorphic, chemically defended mimic are allowed to evolve and disperse. The proportions of the respective model species vary spatially. We use a nonlinear approximation of Müller's number-dependent equations to model a situation where the mortality for either form of the mimic decreases hyberbolically when its local density increases. A first non-spatial analysis confirms that the positive density-dependence makes coexistence of mimetic forms unstable in a single isolated patch, but shows that mimicry of the rarer model can be stable once established. The two-patch analysis shows that when models have different abundance in different places, local mimetic diversity in the mimic is maintained only if spatial heterogeneity is strong, or, more interestingly, if the mimic is not too strongly distasteful. Therefore, mildly toxic species can become polymorphic in a wider range of ecological settings. Spatial dynamics thus reveal a region of Müllerian polymorphism separating classical Batesian polymorphism and Müllerian monomorphism along the mimic's palatability spectrum. Such polymorphism-palatability relationship in a spatial environment provides a parsimonious hypothesis accounting for the observed Müllerian polymorphism that does not require quasi-Batesian dynamics. While the stability of coexistence depends on all factors, only the migration rate and strength of selection appear to affect the level of diversity at the polymorphic equilibrium. Local adaptation is predicted in most polymorphic cases. These results are in very good accordance with recent empirical findings on the polymorphic butterflies Heliconius numata and H. cydno.     

Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest

1. Birds are considered to be the primary selective agents for warning colouration in butterflies, and select for aposematic mimicry by learning to avoid brightly coloured prey after unpleasant experiences. It has long been thought that bright colouration plays an important role in promoting the avoidance of distasteful prey by birds. 2. The hypothesis that warning colouration facilitates memorability and promotes predator avoidance was tested by means of a field experiment using distasteful model butterflies. Artificial butterflies with a Heliconius colour pattern unknown to local birds were generated using bird vision models, either coloured or achromatic, and hung in tree branches in a tropical forest. Two sequential trials were conducted at each site to test avoidance by naïve and experienced predators. 3. There was a significant reduction in predation in the second trial. Also, coloured models were attacked less than achromatic models. Specifically, coloured butterflies were attacked significantly less in the second trial, but there was no significant decrease in predation on achromatic models. 4. The present results imply an important role for colour in enhancing aversion of aposematic butterflies. It has also been demonstrated that previous experience of distasteful prey can lead to enhanced avoidance in subsequent trials, supporting mimicry theory.     

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.     

Responses of great tits Parus major to small tortoiseshells Aglais urticae in feeding trials; evidence of aposematism

Abstract.  1. The small tortoiseshell Aglais urticae (Lepidoptera, Nymphalidae) is one of several red-coloured butterflies and moths that are active in early spring in Norway. It has been suggested that tortoiseshells may be warningly coloured and unpalatable to birds, however no experiments have been carried out to test this hypothesis.
2. The reactions of wild-caught great tits Parus major (Paridae) when offered dead specimens of the tortoiseshell and four palatable control species were studied. Two experiments were carried out. In expt 1, only intact prey was presented to the birds. In expt 2, the birds were offered only experimentally de-winged prey. Hence, in expt 2, it was possible to explore to what extent the birds' reaction to the prey offered to them in expt 1 could be explained as a reaction to visual stimuli from the wings of the prey.
3. In both experiments, tortoiseshells were attacked hesitantly, eaten slowly, and rejected often compared with controls, providing evidence that tortoiseshells are mildly distasteful to great tits. Moreover, all birds were more hesitant to attack intact than de-winged tortoiseshells, while there was no such effect for control prey, indicating a warning effect associated with the butterfly wings. There were also indications of avoidance learning in the birds to the presented tortoiseshells. These results are consistent with the idea of aposematism.     

Optimal diet selection,frequency dependence and prey renewal

This paper extends existing models of frequency-dependent diet selection by considering the optimal diet selection of a predator feeding upon prey populations which can be depleted but are also capable of renewal (e.g. immigration, growth, or reproduction). This model and existing models which include prey depletion, predict partial-preference and a generic diet preference for the commonest prey types (apostatic selection). Unlike previous diet selection models, it is found that the optimal diet selection of an individual predator can be to favour the rarest prey type (anti-apostatic selection) when encounter rates are high, even if the individual prey do not differ in their nutritional value. Studies have demonstrated that predators generally show apostatic selection, even when all prey have the same nutritional value. Anti-apostatic selection has also been observed when prey are crowded, and therefore at high density, consistent with the idea of high encounter rates. This anti-apostatic diet selection has previously been proposed as evidence for the use of prey search images by a predator, or variation in individual prey preference. In this paper it is suggested that prey renewal is a further factor, often confounded in experiments, which could favour anti-apostatic selection.     

The influence of density on frequency-dependent food selection: a comparison of four experiments with wild birds

We compare the results of four experiments, conducted at different times and with different protocols, that explored the relationship between frequency-dependent selection and prey density in wild birds feeding on artificial populations of coloured baits. One (experiment 4) used pastry baits that differed only in the presence or absence of a red stripe, and this experiment provided no evidence for any kind of selective behaviour. The other three experiments used green and brown baits, and they all provided evidence for a trend towards increasing anti-apostatic selection with high densities (>100 baits m^–2). However, one of these (experiment 3) provided no evidence for frequency-dependent selection at low densities (0.5–20 baits m^–2), while the other two experiments concurred in suggesting a trend towards increasing apostatic selection with low densities (down to 2 baits m^–2). Together, these experiments both support and qualify the published findings of experiment 1 that frequency- dependent selection by wild birds on bait populations is modified by density. Experiment 4 indicates that frequency-dependent selection may break down entirely if bait types are too similar, while experiment 3 indicates that some details of this trend with density will depend either on the protocol used or on exogenous changes in the birds’ feeding behaviour. Received: 1 September 1999 / Accepted: 22 March 2000     

A junk-food hypothesis for gannets feeding on fishery waste

Worldwide fisheries generate large volumes of fishery waste and it is often assumed that this additional food is beneficial to populations of marine top-predators. We challenge this concept via a detailed study of foraging Cape gannets Morus capensis and of their feeding environment in the Benguela upwelling zone. The natural prey of Cape gannets (pelagic fishes) is depleted and birds now feed extensively on fishery wastes. These are beneficial to non-breeding birds, which show reduced feeding effort and high survival. By contrast, breeding gannets double their diving effort in an attempt to provision their chicks predominantly with high-quality, live pelagic fishes. Owing to a scarcity of this resource, they fail and most chicks die. Our study supports the junk-food hypothesis for Cape gannets since it shows that non-breeding birds can survive when complementing their diet with fishery wastes, but that they struggle to reproduce if live prey is scarce. This is due to the negative impact of low-quality fishery wastes on the growth patterns of gannet chicks. Marine management policies should not assume that fishery waste is generally beneficial to scavenging seabirds and that an abundance of this artificial resource will automatically inflate their populations.     

Some population consequences of variation in preference among individual predators

A number of foraging studies have demonstrated that populations of predators rarely consist of individuals with identical preferences for particular types of prey. Variation among predators can lead to frequency-dependent changes in population preference, because those predators mat prefer the rarer type of prey generally have the greatest influence on population preference. In this study we develop a series of theoretical models which demonstrate how anti-apostatic selection (i.e. selection against the rare form) can arise out of (a) bimodal and (b) normal variation in preference among individuals of the same species. We show that population level anti-apostatic selection can occur even when individual predators show pro-apostatic selection (i.e. selection against the common form). Furthermore, patterns of population prey selection that arise out of variation in preference can potentially be pro-apostatic over one range of relative densities and anti-apostatic over another range of relative densities. Finally, we examine a case study involving predation by female waterboatmen Notonecta glauca and show that the variation in preference in this species is large enough to generate higher anti-apostatic selection than would be expected from the diet selected by the average individual.     

Does prey dispersion affect frequency-dependent predation by wild birds?

Despite the fact that the vast majority of natural prey items are dispersed in a non-random manner, few studies of frequency-dependent selective predation have explicitly examined the effect of prey dispersion on selectivity. We examined the effect of prey dispersion on the direction and strength of frequency-dependent selection by wild birds feeding on artificial prey (green or brown pastry baits). In a series of four experimental manipulations, we tested for the occurrence of frequency dependence with two different dispersion patterns (random or clumped). Manipulations were carried out at one of two absolute densities (25 prey m⁻² or 100 prey m⁻²), and were repeated at different sites in Southampton, England and Aljarafe, Spain. Our results suggest that prey dispersion has no effect on either frequency-dependent or -independent preferences. One possible explanation for this is that the birds had virtually complete information about prey frequencies at the relatively high densities used and based their preferences on their overall perception of availability. However, we cannot rule out the possibility that dispersion may influence selectivity when prey are cryptic or available at lower absolute densities. Although there was no effect of dispersion, frequency-dependent selection was, overall, significantly anti-apostatic (i.e. rare baits were more preferred than common baits). This anti-apostatic effect was stronger in Southampton than Aljarafe and stronger at 100 prey m⁻² than 25 prey m⁻². The differences in the strength of selection between the two locations was interpreted in terms of (i) whether the avian predators foraged in flocks or not, and (ii) the number of different species present (and, consequently, the variation in preference among individual birds). Received: 21 December 1996 / Accepted: 26 February 1997     

A discrete time stochastic model of a two prey, one predator species interaction

A stochastic discrete time model of a two prey, one predator interaction, an extension of one and two species models proposed by Leslie (1958) and Leslie and Gower, 1958, Leslie and Gower, 1960, is studied. Monte Carlo simulations and the stability properties of the analogous continuous time deterministic model suggest the following hypotheses. (1) The two prey, one predator interaction is in general unstable. The range of parameters allowing coexistence of all three species is small. (2) Deterministically the predator always survives. (3) If the parameters defining the effects of density on the rates of population growth are large, the simulations lead to the rapid extinction of all three species or all but one of the prey species even if the interaction is deterministically stable. (4) The outcome of this three species interaction is largely probabilistic over a wide range of parameters. (5) A prey species with a competitive advantage over a second prey species may still find it difficult to invade and displace the second prey species if the density of the second prey species is high. Increasing the density of the predator offsets this numerical advantage somewhat. (6) The introduction of a predator common to two noncompeting species of prey usually leads to the extinction of one of the prey species. (7) In a stable two prey, one predator interaction the fluctuations of the two prey species are nonperiodic and erratic. The fluctuations of the rarer prey species are damped relative to the commoner species and the fluctuations of the rarer prey species behave as if the series has no fixed mean abundance. The predator population fluctuates with a remarkably constant period. The relevance of these hypotheses to the problem of relating population stability and persistence with the number of species in a community is discussed.     

The evolution of warning signals as reliable indicators of prey defense

It is widely argued that defended prey have tended to evolve conspicuous traits because predators more readily learn to avoid defended prey when they are conspicuous. However, a rival theory proposes that defended prey have evolved such characters because it allows them to be distinguished from undefended prey. Here we investigated how the attributes of defended (unprofitable) and undefended (profitable) computer-generated prey species tended to evolve when they were subject to selection by foraging humans. When cryptic forms of defended and undefended species were similar in appearance but their conspicuous forms were not, defended prey became conspicuous while undefended prey remained cryptic. Indeed, in all of our experiments, defended prey invariably evolved any trait that enabled them to be distinguished from undefended prey, even if such traits were cryptic. When conspicuous mutants of defended prey were extremely rare, they frequently overcame their initial disadvantage by chance. When Batesian mimicry of defended species was possible, defended prey evolved unique traits or characteristics that would make undefended prey vulnerable. Overall, our work supports the contention that warning signals are selected for their reliability as indicators of defense rather than to capitalize on any inherent educational biases of predators.     

Aposematism: what should our starting point be?

The evolution of aposematism is considered to be a major evolutionary problem because if new aposematic forms emerged in defended cryptic populations, they would face the dual problems of rarity and conspicuousness. We argue that this commonly assumed starting point might not have wide validity. We describe a novel evolutionary computer model in which prey evolve secondary defences and become conspicuous by moving widely over a visually heterogeneous habitat. Unless crypsis imposes high opportunity costs (for instance, preventing prey from efficient foraging, thermoregulation and communication), costly secondary defences are not predicted to evolve at all. However, when crypsis imposes opportunity costs, prey evolve secondary defences that facilitate raised behavioural conspicuousness as prey exploit opportunities within their environment. Optimal levels of secondary defence and of behavioural conspicuousness increase with population sizes and the costs imposed by crypsis. When prey are already conspicuous by virtue of their behaviours, the evolution of aposematic appearances (bright coloration, etc.) is much easier to explain because aposematic traits add little further costs of conspicuousness, but can bring large benefits.     

Do predators limit the abundance of alternative prey? Experiments with vole‐eating avian and mammalian predators

Predation has been invoked as a factor synchronizing the population oscillations of sympatric prey species, either because predators kill prey unselectively (the Shared Predation Hypothesis; hereafter SPH), or because predators switch to alternative prey after a density decline in their main prey (the Alternative Prey Hypothesis; APH). A basic assumption of the APH is that the impact of predators on alternative prey depends more on the density of main prey than on the predator/alternative prey ratio. Both SPH and APH assume that the impact of predators on alternative prey is at least periodically strong enough to depress prey populations. To examine these assumptions, we utilized data from replicated field experiments in large areas where we reduced the breeding densities of avian predators during three years and the numbers of least weasels (Mustela nivalis) in two years when vole populations declined. In addition, we reduced the breeding densities of avian predators in two years when vole populations were high. The reduction of least weasels increased the abundance of their alternative prey, small birds breeding on the ground, but did not affect the abundance of common shrews (Sorex araneus). In years when vole populations declined, the reduction of avian predators increased the abundance of their alternative prey, common shrews and small birds. Therefore, vole‐eating predators do at least periodically depress the abundance of their alternative prey. At high vole densities, the reduction of avian predators did not increase the abundance of common shrews, although the ratio of avian predators to alternative prey was similar to years when vole populations declined, which supported APH. In contrast, the abundance of small birds increased after the reduction of avian predators also at high vole densities, which supported SPH. The manipulations had no obvious effect on the number of game birds, which are only occasionally killed by these small‐sized predators. We conclude that in communities where most predators are small or specialize on a single prey type, the synchronizing impact of predation is restricted to a few similar‐sized species.     

When cormorants go fishing: the differing costs of hunting for sedentary and motile prey

Cormorants hunt both benthic (sedentary) and pelagic (motile) prey but it is not known if the energy costs of foraging on these prey differ. We used respirometry to measure the costs of diving in double-crested cormorants (Phalacrocorax auritus) foraging either for sedentary (fish pieces) or motile (juvenile salmon) prey in a deep dive tank. Short dives for sedentary prey were more expensive than dives of similar duration for motile prey (e.g. 20% higher for a 10s dive) whereas the reverse was true for long dives (i.e. long dives for motile prey were more expensive than for sedentary prey). Across dives of all durations, the foraging phase of the dive was more expensive when the birds hunted motile prey, presumably due to pursuit costs. The period of descent in all the dives undertaken appears to have been more expensive when the birds foraged on sedentary prey, probably due to a higher swimming speed during this period.     

The influence of density on frequency-dependent selection by wild birds feeding on artificial prey

Previous work has demonstrated frequency-dependent selection by wild garden birds when feeding on green and brown pastry ''baits''. When the density of baits is low, the common colour is eaten disproportionately more than the rare colour (apostatic selection), and when the density is very high, the rare colour is eaten disproportionately more than the common (anti-apostatic selection). We explored the relationship between frequency-dependent predation and density in an experiment at 16 separate sites, using four levels of density and two frequencies of green and brown. Analysis of estimates of log-relative risk ratios showed little evidence for frequency-independent selection, but frequency-dependent selection changed gradually from apostatic at low density to anti-apostatic at high density. The validity of these conclusions in terms of individual bird behaviour was confirmed by Monte-Carlo simulations. We thus conclude that selection by wild birds feeding on green and brown artificial prey is frequency dependent, and that the strength and direction of this selection changes with prey density in a gradual and predictable manner.     

Importance of conspicuous colours in warning signals: the great tit’s (Parus major) point of view

Few studies have dealt with the importance of colours per se in warning signalling, with the use of a broader array of different colours. We tested the reactions of great tits (Parus major) to colour modifications (red, orange, yellow, white, blue, violet, and green) of the warning signal of the red firebug (Pyrrhocoris apterus), preserving its typical black pattern. We used the edible Guyana spotted roach (Blaptica dubia) as the prey, each of which carried a paper sticker shield of a particular colour on its back. With such prey, the effects of the other traits of the red firebug (e.g. shape of the legs and antennae or chemical signals) on the birds’ reactions were removed. All of the conspicuous forms of the prey, possessing a black pattern, were protected against great tits better than the non-patterned brown control form. The level of protection decreased from those forms with colours similar to the model and commonly occurring in warning signals in nature (red, orange, yellow), through other conspicuous colours rarely occurring in warning signals in nature (white, violet, blue), to the colour which usually occurs as cryptic in nature (green). In the green form, repeated encounters were necessary to reach avoidance. Avoidance learning came to pass despite the fact that the presented prey was neither inedible nor distasteful.