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.     

Polymorphism in Cepaea Hortensis in marginal populations in Spain

Cepaea hortensis (Mull) is found in Spain only in the western part of the Iberian mountain range. This is the southernmost limit of its range. The most frequent colour is yellow, brown being very rare. The most frequent band patterns are 12345, fused banded and unbanded. There are associations between maximum and minimum temperatures and pink and effectively unbanded yellow phenotypes. The populations may be grouped into two zones, one located in the north and the other in the south of the sampled area. Visual predation was not observed. The marginal populations studied by us were compared with others from Northern Europe, and it was observed that pink snails are more frequent at the southern limit, and unbanded ones at the northern limit. This was interpreted as a climatic selection.     

Distribution patterns of morph frequencies in the snail Cepaea hortensis in Iceland

In Iceland Cepaea hortensis Müll. reaches its northern limit of distribution occurring in restricted areas along the south coast. Samples of snails collected along steep cliffs in two such restricted areas were effectively monomorphic for shell colour (yellow), but were polymorphic for banding pattern and revealed strong area effects. In both localities samples from sites facing east contained varying frequencies of unbanded snails whereas in ecologically similar sites facing south unbanded were absent. In an experimental population released at a south-facing site unbanded snails failed to become established whereas banded individuals survived and bred. It is suggested that the area effects are maintained through non-visual (most likely climatic) selection though other possibilities cannot be ruled out.     

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.     

Disequilibrium in some Cepaea populations

Phenotypic disequilibrium is a measure available, along with morph frequency, in many published sets of sample data recording the polymorphism of shell colour and pattern in the snail Cepaea nemoralis. The relation of disequilibrium to morph frequency for the colour (pink/yellow) and banding (unbanded/banded) loci has been examined for a large and widespread set of data. The direction of disequilibrium is a function of frequency at the two loci in a way that suggests that selection favours combinations of common morphs, whichever they are. This could indicate that such combinations are common because they have been selected. The data are therefore consistent with the proposal that populations are generally subject to selection of varying directions at different places and times, acting on the phenotype. In combination with migration, such selection could lead to prolonged polymorphism.     

Gene frequency changes in Cepaea snails on the Marlborough Downs over 25 years

In 1985 we resurveyed the sites on the Marlborough Downs in southern England at which Cain and Currey in 1960/61 sampled Cepaea snails and thence introduced the term 'area effects' to describe large areas of uniform morph frequency. Some sites no longer harboured Cepaea and at others the species composition had changed, with a general spread of Cepaea hortensis at the expense of Cepaea nemoralis. The majority, however, permitted comparison of morph frequencies between the two surveys. In C. nemoralis, we detected a significant overall decrease in the frequency of the brown morph and estimate selection as 5–9% per generation. There was no apparent change in frequencies of banded morphs. In C. hortensis we detected a significant overall increase in the frequency of unbanded shells (1–3% selection per generation) and an almost significant decrease in the frequency of fusions within the banded class. There was insufficient colour polymorphism in C. hortensis to allow analysis of colour morph frequencies. These changes—all in the direction of reduced absorption of solar energy—resemble others detected in both species at other localities in southern England. Possible explanations include large-scale climatic effects and changes in vegetation.     

Selection by passerine birds is anti-apostatic at high prey density

Most of the results from past experiments with wild birds and green and brown pastry 'baits' have suggested that disproportionately more of the rare forms are eaten when bait density is high (i.e. selection is anti-apostatic). In two separate series of experiments we presented birds with dishes containing 270 baits of one colour and 30 of another. In series I, five different pairs of colours were presented simultaneously to wild birds at two sites. One colour of each pair was common at one site and the same colour was rare at the other site. After 35 days the ratios of the colours were reversed and the dishes were presented for another 35 days. There was a statistically significant tendency for the colours to be at a higher risk when rare. In series II, three caged blackbirds were offered green and brown baits in two dishes simultaneously; in one dish green was rare and in the other brown was rare. Selection over 6 days was anti-apostatic for all three birds combined but the data proved heterogeneous both between and within individuals. At any one time, each bird tended to concentrate on one colour, irrespective of whether that colour was rare or common. We believe that this behaviour leads to anti-apostatic selection, as has been observed in these and other experiments with pastry prey.     

Temperature effects on energy metabolism in banded and unbanded morphs of the snail Cepaea hortensis Müll

Summary Energy metabolism (oxygen consumption) in acclimated juvenile yellow banded and unbanded Cepaea hortensis Müll. was measured at 5°, 10°, 15°, 20°, and 25°C with Englemann respirometers. Metabolic rates were also measured after abrupt temperature changes from 5° to 20° and from 25° to 10°C.Energy metabolism in the two morphs was significantly different at 5° and 20°C. The metabolism/temperature curve in the banded morph was relatively flat with reduced regulating power at 20°C. The yellow unbanded form had a lower metabolism at 5°C, but between 15° and 25°C the curve was flat and indicated good regulating ability. A sudden decrease in experimental temperature gave significant response in both morphs. The effect of abrupt temperature increase was significant only in unbanded snails. Banded and unbanded snails thus displayed different adaptation strategies.Differential heating because of different pigmentation is discussed. The increase in metabolic rate with increased temperature was highest in the yellow unbanded morph. The effects were small and probably overridden by the influences of acclimation and behavior.The use of energetic parameters in ecological genetics is considered. It is suggested that the cohort producing most progeny with lowest energetic cost per energy unit of offspring is the better adapted to the local environment.     

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.     

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.     

Wild birds prefer the familiar morph when feeding on pastry-filled shells of the landsnail Cepaea hortensis (Müll.)

Colour polymorphisms in prey could be maintained if predators concentrate on common morphs and confer a selective advantage on rare morphs. We describe experiments to test whether wild birds feed on pastry-stuffed shells of Cepaea hortensis in a manner that might lead to such apostatic selection. The birds were first given a 'pre-training' choice test of a shell population with equal numbers of yellow unbandeds and yellow five-bandeds; they were then trained on one morph alone, given a second choice test, trained on the other morph and, finally, given a third choice test. The birds preferred five-bandeds in five of the six pre-training tests. In all six experiments the first training session increased the birds' preferences for the morph that was familiar. The results were less clear-cut when selection during pre-training was compared with selection after the second training session. However, a comparison between selection after each of the two training sessions showed that in all six experiments the results were in the direction predicted from the hypothesis that familiar morphs are preferred. This set of experiments is one of the few in which behaviour which could lead to apostatic selection has been tested with morphs that differ in pattern. The findings support the idea that polymorphism in Cepaea could be maintained by apostatic selection.     

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.     

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     

Apostatic selection by song thrushes (Turdus philomelos) feeding on the snail Cepaea hortensis

There is no direct evidence that predators exert apostatic selection (the systematic overpredation of commoner forms) on live, naturally polymorphic prey. This study tested whether captive song thrushes ( Turdus philomelos ) select apostatically when presented with dimorphic populations of yellow five-banded and yellow unhanded morphs of the snail Cepaea hortensis. Four thrushes were used. Two were presented with a 9: 1 ratio of five-bandeds to unbandeds and two were presented with 1:9 ratios. Each thrush was given four trials in succession. In each trial 30 snails were presented and the trial was stopped when 15 had been eaten. There were no differences in shell size between morphs or between eaten and uneaten snails of each morph. Three thrushes selected apostatically and one thrush exerted virtually no selection. Overall, there was statistically significant apostatic selection.     

Lake Erie water snakes revisited: Morph- and age-specific variation in relative crypsis

Summary Populations of water snakes (Nerodia sipedon insularum) on islands in western Lake Erie are variable in colour pattern, consisting of unbanded, intermediate, and banded morphs. In contrast, mainland populations (N. s. sipedon) consist solely of banded morphs. Previous investigators hypothesized that natural selection favoured unbanded morphs on exposed island shorelines and banded morphs in overgrown mainland habitats and that gene flow from mainland populations was responsible for the persistence of banded morphs on islands. To clarify the potential role of natural selection, I quantified relative crypsis among morphs and age classes of water snakes by comparing the size of patches making up their colour patterns with the size of patches in island and mainland backgrounds. This analysis reveals that if unbanded morphs are more cryptic than intermediate and banded morphs on islands, it is only in the young-of-the-year age class. For older snakes on islands and for all snakes on the mainland, unbanded morphs are consistently less cryptic than intermediate and banded morphs. Given these results, the net direction of selection in island populations should depend on the intensity of predation on different age classes of snakes. Overall, selection may favour unbanded morphs (e.g. if predation occurs primarily on young-of-the-year), intermediate and banded morphs (e.g. if predation occurs primarily on older snakes), or be weak or absent (e.g. certain combinations of predation on young-of-the-year and older snakes). Using estimates of relative crypsis to guide reanalysis of morph frequency data, I find support for the hypothesis that unbanded morphs are favoured by natural selection in island populations.     

Activity and weight loss in relation to solar radiation in the polymorphic land snail Cepaea nemoralis

Shell spectral reflectance, activity and weight loss in the land snail Cepaea nemoralis were examined to test whether solar radiation has different effects on the behavioural and physiological responses of different morphs. A uniform area from the empty shells of different morphs was cut and a spectrophotometer was used to measure the spectral reflectance at wavelengths from 220 nm to 800 nm. Snails were put into cages made of mesh hardware cloth, and their activities were observed from dawn onwards on two hot, dry days. Weight loss of snails under shade and under direct sunlight was also measured.
The results show that unbanded morphs reflect more light than five-banded ones, but the yellow morphs reflect only a little more than pink morphs. Five-banded morphs became inactive more quickly than unbanded ones from dawn onwards, but the differences in activity patterns were not significant between pink and yellow morphs. There are significant differences in percent weight loss between snails placed under direct sunlight and under shade. The weight loss of different morphs under shade was not statistically different. But when exposed to sunlight, five-banded morphs lost more weight than pink and yellow unbanded morphs.
Because of their lower reflectance of solar radiation, the five-banded morphs are, in a hot, arid climate, at a selective disadvantage compared to unbanded morphs. However, they can avoid such selective disadvantage by actively seeking a shaded area, as all other morphs do in the field. Such behavioural habitat selection could help the maintenance of genetic polymorphisms in natural populations.     

Selection and disequilibrium in Cepaea nemoralis

The snail Cepaea nemoralis (L.) is usually polymorphic for linked loci conferring pink or yellow shell ground colour and banding or lack of bands. An unlinked locus, mid‐banded, modifies the appearance of banded shells. These characters have a very wide range of frequencies across the species range and even within limited areas. In Britain, frequencies differ between populations from shaded woodland habitats and those from closely adjacent open habitats. Using data from the Evolution MegaLab Project, it is shown that the greater frequency of pink unbanded in shaded habitats is associated with a greater excess of the favoured allele combinations, measured as linkage disequilibrium. Examination of the relationship of disequilibrium to allele frequency in samples from the full geographical range and all habitats and climates shows that, in general, the allele combinations at high frequencies are in gametic excess. This suggests that selection tends to diversify rather than move frequencies towards stable equilibria. The result is important in relation to the as yet unresolved question how the polymorphism is maintained. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

COLOR PATTERN POLYMORPHISM IN THE LAKE ERIE WATER SNAKE,NERODIA SIPEDON INSULARUM

Populations of the water snake, Nerodia sipedon, on islands in western Lake Erie are polymorphic for color pattern. These populations include banded, intermediate, and unbanded morphs while surrounding mainland populations consist solely of the banded morph. The hypothesis that this polymorphism is maintained by strong selection and migration pressures is widely accepted. Unbanded morphs are apparently more cryptic along island shorelines while banded morphs are more cryptic on the mainland. Migration of banded morphs from the mainland explains their persistence in island populations. Data collected in a capture-mark-recapture program on six islands provide no evidence of differential selection among morphs; morph frequencies do not differ among age classes, between once-captured and multiply-captured snakes, or between scarred and unscarred snakes. Furthermore, herring gulls, the most common snake predators in the island area, appear to detect banded and unbanded model snakes with equal ease. High site fidelity of water snakes and the distribution of morphs among islands suggest that migration from the mainland is not common. However, islands close to each other are similar in morph frequency, and water snakes have colonized islands elsewhere in the Great Lakes, indicating that some migration does occur. Recently, the frequency of banded morphs has increased in island populations while adult population sizes have declined. This increase in banded morphs is interpreted as reflecting an increased impact of migration from the mainland into these reduced populations. One scenario for the evolution and maintenance of this polymorphism is that selection was important in establishing unbanded morphs in island populations as they became isolated from the mainland. As populations declined to their present size, the impact of migration from the mainland increased and is now swamping the effect of selection. Further declines in island population size may result in fixation of the banded morph.     

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     

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.