Predator-prey relationships and the evolution of colour polymorphism: a comparative analysis in diurnal raptors

Genetically based variation in coloration occurs in populations of many organisms belonging to various taxa, including birds, mammals, frogs, molluscs, insects and plants. Colour polymorphism has evolved in raptors more often than in any other group of birds, suggesting that predator–prey relationships was a driving evolutionary force. Individuals displaying a new invading colour morph may enjoy an initial foraging advantage because prey have difficulties in learning the colour of a rare morph (apostatic selection), or because morphs provide alternative foraging benefits allowing differently coloured individuals to exploit distinct food niches (disruptive selection). Plumage polymorphism should therefore have evolved in species that prey upon animals having the physiological ability to distinguish between differently coloured predators but also to flee once a predator has been detected. From this assumption, we can predict that closely related polymorphic and monomorphic species prey upon different animals. They may also differ in morphology, because foraging upon different prey may require different foraging modes, and in turn different morphological structures. We tested these two predictions in a comparative study of raptors. As expected, polymorphic and monomorphic species had a different diet, and there was a difference in wing length between polymorphic and monomorphic species within two genera ( Buteo and Accipiter ). Across all raptors for which phylogenetic relationships are known, polymorphic species preyed more often upon mammals than did monomorphic ones. These two types of raptor did not differ in the frequency of birds, insects and reptiles in their diets. We discuss these results in the light of the hypothesis that predator–prey relationships played a role in the evolution of colour polymorphism. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 565–578.     

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.     

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.     

Apostatic selection on prey that match the background

There is good experimental evidence that predators often remove disproportionately more of the common prey types. This 'apostatic selection' could maintain colour polymorphisms within prey species. In nature, morphs of many species appear to match components in the background, but most of the experiments that have tested apostatic selection have used prey that were conspicuous. In work described in this paper, wild birds at one site were presented a random order of 51 experiments. Seventeen frequencies of orange and grey pastry prey were presented on each of three types of background: a hessian sheet scattered with either orange and grey stones (the 'matching' background), or lilac and yellow stones, or green stones (two sorts of 'control' background). Each experiment consisted of four trials in succession and the numbers of the two colours eaten in each trial were recorded when about half the total prey had been eaten. Two methods of graphical analysis revealed that apostatic selection occurred on the prey on all three backgrounds, but was strongest in the grey/orange one. This last result must have been caused by some effect of the match between prey and background colour, and behavioural explanations are suggested. It is unclear whether the prey were exhibiting 'crypsis' or 'masquerade'.     

Fish stocking creates an ecological trap for an avian predator via effects on prey availability

In anthropogenic landscapes animals may be lured into low‐quality habitats where they survive or reproduce poorly (‘ecological traps’). I investigated breeding habitat selection in relation to intra‐seasonal changes in food availability and reproductive output in red‐necked grebes Podiceps grisegena, a size‐limited predator, of common carp Cyprinus carpio ponds. Carp farms constitute highly heterogeneous habitat mosaics due to separate stocking of different age/size fish. Pond features significant for grebe settling decisions, i.e. hydroperiod and emergent vegetation cover, had no obvious effects on prey abundance for chicks and on fledging success. Breeding grebes avoided ponds containing fish too large for them to ingest but exhibited little preference between ponds with medium‐sized one‐year‐old carp that could be exploited by pre‐laying birds, and ponds designated for young‐of‐the‐year carp, where only invertebrates and amphibians were available as prey in early spring. Red‐necked grebes settling on ponds with medium‐sized fish failed to predict future shifts in interactions with carp stocks; carp exceeded the prey‐size threshold of chicks and adversely affected their non‐fish prey levels. The resulting food shortage led to severe egg‐to‐fledging mortality rates compared to fishless ponds or those containing young‐of‐the‐year fish. This study shows that waterbirds vulnerable to competition from fish can risk maladaptive habitat selection due to unrecognised spatial and temporal variation in food resources caused by fish stocking practices. Ecological traps created by perturbations to trophic interactions may be common but difficult to detect because altered dynamics of trophic resources can affect wildlife indirectly. As with other types of ecological traps, manipulation of habitat features identified as attractive cues for settling animals, but not related to critical food resources, may help to reduce perceptual pitfalls. For example, wetland management to mitigate trap effects driven by commercially stocked fish should preserve abundant emergent vegetation in habitats with weak fish impact and extend their hydroperiod.     

Polymorphism of melanic ladybirds maintained by frequency-dependent sexual selection

Sexual selection, whether by female preference or male competition, is almost inevitably frequency-dependent. Female preference gives rise to a 'rare male effect', by which the rarer male phenotypes gain a relatively greater selective advantage. In addition to this effect, the proportion of females expressing a preference may also be frequency-dependent.
Frequency-dependent expression of mating preference can arise in at least two ways: (1) when females encounter a succession of courting males while searching for a male they prefer; (2) when females chose a male from within a lek. Models of mating behaviour reveal a clear distinction between the frequency dependence in the expression of female preference and the frequency dependence in the consequent selection of the males. When expression of preference is highly dependent on frequency, the selection of males is constant or only slightly frequency-dependent: constant expression of preference produces high frequency dependence of selection. Analysis of general models shows that genetic polymorphisms can be maintained under a wide range of conditions.
The ladybird, Adalia bipunctata , is polymorphic for several melanic and non-melanic phenotypes. Females have a genetically determined preference for melanic males. Non-melanic phenotypes mate assortatively. By estimating the parameters of a detailed model of natural selection, sexual selection and assortative mating, it has been shown that the Adalia bipunctata polymorphism will be maintained at frequencies observed in the wild.     

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.     

Feeding Experience Modifies the Assessment of Ambush Sites by the Timber Rattlesnake, a Sit-and-Wait Predator

To effectively ambush prey, sit‐and‐wait predators must locate sites where profitable prey are likely to return. One means by which predators evaluate potential ambush sites is by recognizing high‐use areas through chemical cues deposited inadvertently by their prey. However, it is unknown whether ambush predators can use chemical cues associated with past prey items in the assessment of potential ambush sites. I examined selection of ambush sites by timber rattlesnakes (Crotalus horridus) exposed to trails made from chemical extracts of the integument of various prey species. I evaluated the role of feeding experience in ambush site selection by comparing the behavior of timber rattlesnakes before and after feeding experience with different sized prey items. Timber rattlesnakes are more likely to select ambush sites adjacent to chemical trails from prey with which they have had feeding experience, but only those fed relatively large prey showed an increase in responsiveness. Increased responsiveness after feeding experience was exhibited in experiments using integumentary extracts of mammals (the natural prey of timber rattlesnakes), but not in those using extracts of fish. These results indicate that ambush predators may learn to recognize chemicals on the integument of profitable food items, and use that experience when subsequently selecting ambush sites. Additionally, these findings provide evidence that size‐dependent predation by snakes may be, in some species, a result of active prey selection.     

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.     

Jaw and hyolingual movements during prey transport in varanid lizards: effects of prey type

The ability to modulate feeding kinematics in response to prey items with different functional properties is likely a prerequisite for most organisms that feed on a variety of food items. Variation in prey properties is expected to reveal variation in feeding function and the functional role of the different phases in a transport cycle. Here we describe the kinematics of prey transport of two varanid species, Varanus niloticus and Varanus ornatus. These species were selected for analysis because of their highly specialised hyolingual system and food transport mechanism (inertial food transport). In these animals, tongue and hyoid movements are expected to make no, or only a minor, contribution to prey transport. We observed statistically significant prey type effects that could be associated with prey properties such as mass, size and mobility. These data show that both species are capable of modulating the kinematics of food transport in response to different prey types. Moreover, not only the kinematics of the jaws were modulated in response to prey characteristics but also the anterior/posterior movements of the tongue and hyoid. This suggests a more important role of the tongue and hyolingual movements in these animals than previously suspected. In contrast, head movements were rather stereotyped and were not modulated in response to changes in prey type.     

Prey selectivity affects reproductive success of a corallivorous reef fish

Most animals consume a narrower range of food resources than is potentially available in the environment, but the underlying basis for these preferences is often poorly understood. Foraging theory predicts that prey selection should represent a trade-off between prey preferences based on nutritional value and prey availability. That is, species should consume preferred prey when available, but select less preferred prey when preferred prey is rare. We employed both field observation and laboratory experiments to examine the relationship between prey selection and preferences in the obligate coral-feeding filefish, Oxymonacanthus longirostris. To determine the drivers of prey selection, we experimentally established prey preferences in choice arenas and tested the consequences of prey preferences for key fitness-related parameters. Field studies showed that individuals fed almost exclusively on live corals from the genus Acropora. While diet was dominated by the most abundant species, Acropora nobilis, fish appeared to preferentially select rarer acroporids, such as A. millepora and A. hyacinthus. Prey choice experiments confirmed strong preferences for these corals, suggesting that field consumption is constrained by availability. In a longer-term feeding experiment, reproductive pairs fed on non-preferred corals exhibited dramatic reductions to body weight, and in hepatic and gonad condition, compared with those fed preferred corals. The majority of pairs fed preferred corals spawned frequently, while no spawning was observed for any pairs fed a non-preferred species of coral. These experiments suggest that fish distinguish between available corals based on their intrinsic value as prey, that reproductive success is dependent on the presence of particular coral species, and that differential loss of preferred corals could have serious consequences for the population success of these dietary specialists.     

Natural selection in mimicry

Biological mimicry has served as a salient example of natural selection for over a century, providing us with a dazzling array of very different examples across many unrelated taxa. We provide a conceptual framework that brings together apparently disparate examples of mimicry in a single model for the purpose of comparing how natural selection affects models, mimics and signal receivers across different interactions. We first analyse how model–mimic resemblance likely affects the fitness of models, mimics and receivers across diverse examples. These include classic Batesian and Müllerian butterfly systems, nectarless orchids that mimic Hymenoptera or nectar‐producing plants, caterpillars that mimic inert objects unlikely to be perceived as food, plants that mimic abiotic objects like carrion or dung and aggressive mimicry where predators mimic food items of their own prey. From this, we construct a conceptual framework of the selective forces that form the basis of all mimetic interactions. These interactions between models, mimics and receivers may follow four possible evolutionary pathways in terms of the direction of selection resulting from model–mimic resemblance. Two of these pathways correspond to the selective pressures associated with what is widely regarded as Batesian and Müllerian mimicry. The other two pathways suggest mimetic interactions underpinned by distinct selective pressures that have largely remained unrecognized. Each pathway is characterized by theoretical differences in how model–mimic resemblance influences the direction of selection acting on mimics, models and signal receivers, and the potential for consequent (co)evolutionary relationships between these three protagonists. The final part of this review describes how selective forces generated through model–mimic resemblance can be opposed by the basic ecology of interacting organisms and how those forces may affect the symmetry, strength and likelihood of (co)evolution between the three protagonists within the confines of the four broad evolutionary possibilities. We provide a clear and pragmatic visualization of selection pressures that portrays how different mimicry types may evolve. This conceptual framework provides clarity on how different selective forces acting on mimics, models and receivers are likely to interact and ultimately shape the evolutionary pathways taken by mimetic interactions, as well as the constraints inherent within these interactions.     

Learning affects prey selection in larvae of a generalist coccinellid predator

Under natural conditions, generalist predatory insects have to cope with a variety of potential prey species that are not all equally suitable. Under these circumstances, learning may be adaptive if it allows adjustment to variations in resource quality and availability. Under laboratory conditions, we examined the learning ability and memory in the prey selection process of larvae of the predatory coccinellid Coleomegilla maculata ssp. lengi Timberlake (Coleoptera: Coccinellidae). Using choice tests, we studied prey rejection behaviour of C. maculata fourth instars towards prey of different quality and we also tested the influence of hunger and prior experience with other food types on the prey rejection behaviour of coccinellid larvae. Coleomegilla maculata larvae gradually changed their behaviour and rejected low‐quality hosts more frequently, whereas high‐quality hosts were nearly always accepted. After 48 h, the learned behaviour appeared to be partially forgotten. Hunger and experience with other food types prior to the test had little effect on the gradual change of behaviour but the quality of the food ingested influenced the initial level of prey rejection. Our results demonstrate that (1) C. maculata larvae can adjust their prey selection behaviour with experience to reject progressively less suitable prey, and (2) previous experience with other prey types can influence their initial preference.     

Effects of an alien invertebrate species and wave action on prey selection by African black oystercatchers (Haematopus moquini)

Abstract Shorebirds foraging in the intertidal have been shown to exert a significant effect on assemblage level processes; this is particularly true of the oystercatcher–limpet–algae system. The African black oystercatcher (Haematopus moquini) is endemic to the southern African coastline, where it plays a significant role in ecosystem processes as a rocky‐shore predator, especially of mussels and limpets. This understanding was based on studies of a rocky shore environment that has since been considerably modified following invasion of an alien mussel (Mytilus galloprovincialis). This invasion has not only changed the relative proportions of different food types on the shore, but has also greatly increased overall food biomass. We tested the previous model that food selection by oystercatchers reflected prey abundance and that intake by male and female oystercatchers differed owing to bill morphology. We predicted that this difference would persist despite the changed nature of the food base. We also predicted that wave action would modify prey selection as a result of both its influence on prey behaviour and its impact on searching and handling times of the birds. Overall, both sexes consumed more limpets than expected by encounter rate alone, but contrary to prediction, the relative proportions of different prey types taken post invasion did not differ between the sexes. Dietary convergence is interpreted as a result of greatly increased food biomass on the shore, which is also reflected in increased oystercatcher densities since the invasion. Also contrary to prediction there was no evidence that waves acted as indirect modifiers of the interaction between oystercatchers and their prey. The results of this study indicate that models of trophic cascades will need to be altered in the event of a significant change in a trophic level, which then effects behavioural changes in the key predator.     

Six ways in which a foraging predator may encounter options with different variances

We consider the idea that foraging animals seek to achieve a certain threshold intake of food per day rather than maximising mean energy intake. Earlier experiments and theoretical work have shown that under these conditions animals should respond to variance in reward. We identify six possible sources of such variance and produce models for five of them (the sixth is already solved). These models describe (1) whether to feed in habitats possessing small or large prey, (2) whether to feed on clumped or dispersed prey, (3) which prey items to eat, (4) the effects of misidentification of prey selection, (5) whether to feed singly or join a flock and (6) when to move between patches when the travel time between them is variable. The results are often radically different from those of traditional models and we discuss their biological significance.     

The possible role of predator–prey dynamics as an influence on early hominin use of burned landscapes

Foraging in burned areas has been suggested to represent the earliest stage in the use and control of fire by early hominins. Recently burned areas offer immediate foraging benefits including increased search efficiency for high‐ranked food items and decreased hunting opportunities for ambush predators. As such, they provide a triple‐bonus (reduced risk from ambush, ease of terrestrial travel and higher foraging returns) for some primates. However, previous studies have not yet accounted for other types of predators e.g., coursing (endurance predators that can pursue prey over long distances) which were sympatric with hominins and may also have exploited these environments. Behavioral ecology studies on the use of burned landscapes by extant carnivores demonstrate that while some ambush predators avoid recently burned areas, coursing predators do take advantage of their immediate hunting opportunities. Research examining habitat selection by animals under the simultaneous threat of multiple predator species with different modes of hunting, and the diversity of Plio‐Pleistocene carnivore guild is suggestive of two possible evolutionary scenarios in which hominins could either have selected or avoided burned areas (3–2 mya), based on whether ambush or coursing predators were perceived as presenting the greatest risk.     

Prey availability affects territory size,but not territorial display behavior,in green anole lizards

The availability of food resources can affect the size and shape of territories, as well as the behaviors used to defend territories, in a variety of animal taxa. However, individuals within a population may respond differently to variation in food availability if the benefits of territoriality vary among those individuals. For example, benefits to territoriality may differ for animals of differing sizes, because larger individuals may require greater territory size to acquire required resources, or territorial behavior may differ between the sexes if males and females defend different resources in their territories. In this study, we tested whether arthropod abundance and biomass were associated with natural variation in territory size and defense in insectivorous green anole lizards, Anolis carolinensis. Our results showed that both male and female lizards had smaller territories in a habitat with greater prey biomass than lizards in habitats with less available prey, but the rates of aggressive behaviors used to defend territories did not differ among these habitats. Further, we did not find a relationship between body size and territory size, and the sexes did not differ in their relationships between food availability and territory size or behavioral defense. Together, these results suggest that differences in food availability influenced male and female territorial strategies similarly, and that territory size may be more strongly associated with variation in food resources than social display behavior. Thus, anole investment in the behavioral defense of a territory may not vary with territory quality.     

Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey

Chemically defended insects advertise their unpalatability to avian predators using conspicuous aposematic coloration that predators learn to avoid. Insects utilize a wide variety of different compounds in their defences, and intraspecific variation in defence chemistry is common. We propose that polymorphisms in insect defence chemicals may be beneficial to insects by increasing survival from avian predators. Birds learn to avoid a colour signal faster when individual prey possesses one of two unpalatable chemicals rather than all prey having the same defence chemical. However, for chemical polymorphisms to evolve within a species, there must be benefits that allow rare chemical morphs to increase in frequency. Using domestic chicks as predators and coloured crumbs for prey, we provide evidence that birds taste and reject proportionally more of the individuals with rare defence chemicals than those with common defence chemicals. This indicates that the way in which birds attack and reject prey could enhance the survival of rare chemical morphs and select for chemical polymorphism in aposematic species. This is the first experiment to demonstrate that predators can directly influence the form taken by prey's chemical defences.     

Feeding preferences in 2 disjunct populations of tiger snakes, Notechis scutatus (Elapidae)

Variations at both the genetic and phenotypic levels play animportant role in responses to food and food-related stimuli.Knowledge of such variations is crucial to understanding howpopulations adapt to changing environments. We investigatedthe dietary preferences of 2 tiger snake populations and comparedthe responses of diet-naive animals (laboratory-born neonates),diet-controlled animals (laboratory-reared juveniles), and naturaldiet–experienced animals (wild-caught adults) to visualand chemical cues from 6 prey types (mouse, skink, silver gull,chicken, shearwater, and frog). The mainland population inhabitsa swamp, feeds mostly on frogs, and suffers heavy predation.The second population inhabits a small nearby offshore islandwith no standing water (no frogs); feeds mostly on skinks, mice,and, as adults, silver gull chicks; and suffers no known predation.Although different prey are eaten in the 2 populations, adultwild-caught snakes from both populations showed a significantpreference for 3 types of prey (frog, mouse, and chick), irrespectiveof their natural diet. Neonates responded to all prey cues morethan they did to control stimuli in both populations. However,the island neonates showed significantly higher interest insilver gull chick stimuli (the main prey of the island adultsnakes) than did their mainland conspecifics. Laboratory-bredjuveniles displayed behavioral plasticity by significantly increasingtheir response to mice after being fed baby mice for 7 months.We conclude that genetic-based differences in food-related cuesare important in tiger snakes but that they are also capableof behavioral plasticity. Island adult and neonate snakes exhibitedresponses to prey types no longer consumed naturally (frog),suggesting that behavioral characters may have been retainedfor long periods under relaxed selection. Island neonates showeda strong interest in a novel prey item (silver gull). This resultcomplements previous work describing how island snakes havedeveloped the ability to swallow larger prey than usual, aswell as seemingly developing a taste for them.     

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.