Background choice as an anti-predator strategy: the roles of background matching and visual complexity in the habitat choice of the least killifish

Because background matching improves concealment, prey animals have traditionally been expected to prefer parts of the habitat that match their visual appearance. However, empirical support for this is scarce. Moreover, this idea has recently been challenged by an alternative hypothesis: visual complexity of the background impedes prey detection, and hence prey could instead prefer complex parts of the habitat. We used the least killifish to test, with and without predation threat, for the importance of the visual similarity between the fish and the background, and the level of visual complexity of the background. We observed their choice between backgrounds patterned with elements based on the longitudinal black stripe of the fish. Predation risk was important under some circumstances, and induced a preference for a background of matching horizontal stripes compared with mismatching vertical stripes. Interestingly, females under predation threat showed a preference for a complex background of randomly oriented and overlapping stripes compared with matching stripes, whereas males did not discriminate between these two. Additionally, males showed a preference for matching stripes compared with complex shapes, whereas females did not discriminate between these backgrounds. We conclude that matching is important in the choice for safe habitat, but some aspects of visual complexity may override or act together with background matching.     

Can't tell the caterpillars from the trees: countershading enhances survival in a woodland

Perception of the body's outline and three-dimensional shape arises from visual cues such as shading, contour, perspective and texture. When a uniformly coloured prey animal is illuminated from above by sunlight, a shadow may be cast on the body, generating a brightness contrast between the dorsal and ventral surfaces. For animals such as caterpillars, which live among flat leaves, a difference in reflectance over the body surface may degrade the degree of background matching and provide cues to shape from shading. This may make otherwise cryptic prey more conspicuous to visually hunting predators. Cryptically coloured prey are expected to match their substrate in colour, pattern and texture (though disruptive patterning is an exception), but they may also abolish self-shadowing and therefore either reduce shape cues or maintain their degree of background matching through countershading: a gradation of pigment on the body of an animal so that the surface closest to illumination is darker. In this study, we report the results from a series of field experiments where artificial prey resembling lepidopteran larvae were presented on the upper surfaces of beech tree branches so that they could be viewed by free-living birds. We demonstrate that countershading is superior to uniform coloration in terms of reducing attack by free-living predators. This result persisted even when we fixed prey to the underside of branches, simulating the resting position of many tree-living caterpillars. Our experiments provide the first demonstration, in an ecologically valid visual context, that shadowing on bodies (such as lepidopteran larvae) provides cues that visually hunting predators use to detect potential prey species, and that countershading counterbalances shadowing to enhance cryptic protection.     

Empirical tests of the role of disruptive coloration in reducing detectability

Disruptive patterning is a potentially universal camouflage technique that is thought to enhance concealment by rendering the detection of body shapes more difficult. In a recent series of field experiments, artificial moths with markings that extended to the edges of their 'wings' survived at higher rates than moths with the same edge patterns inwardly displaced. While this result seemingly indicates a benefit to obscuring edges, it is possible that the higher density markings of the inwardly displaced patterns concomitantly reduced their extent of background matching. Likewise, it has been suggested that the mealworm baits placed on the artificial moths could have created differential contrasts with different moth patterns. To address these concerns, we conducted controlled trials in which human subjects searched for computer-generated moth images presented against images of oak trees. Moths with edge-extended disruptive markings survived at higher rates, and took longer to find, than all other moth types, whether presented sequentially or simultaneously. However, moths with no edge markings and reduced interior pattern density survived better than their high-density counterparts, indicating that background matching may have played a so-far unrecognized role in the earlier experiments. Our disruptively patterned non-background-matching moths also had the lowest overall survivorship, indicating that disruptive coloration alone may not provide significant protection from predators. Collectively, our results provide independent support for the survival value of disruptive markings and demonstrate that there are common features in human and avian perception of camouflage.     

Novel cost of a sexually selected trait in the rubyspot damselfly Hetaerina americana: conspicuousness to prey

Conspicuousness to predators frequently has been invoked asa cost of sexually selected traits, but conspicuousness to preyhas not We tested for the latter using rubyspot damselflies(Hetaerina americana) as the predator. Previous work on thisspecies showed that the red spots on male wings are intrasexuallyselected and reduce survival. Since female wings lack red spots,we first compared male and female weight gain rates per unithunting time. Females gained weight significandy faster thanmales in both mg per hour and relative to body weight. We thencompared the weight gain rates of females painted with red wingspots to those of control females painted with clear ink ornot manipulated. Controls gained weight significandy fasterthan red-painted females. Behavioral observations revealed thatred females attempted to capture prey at normal rates and experiencednormal rates of agonistic interference from conspecifics ofboth sexes. Nevertheless, red females captured fewer prey perminute and per capture attempt than did sham-manipulated andunmanipulated controls. We infer that the red spots reducedfemale weight gain rates by increasing their visibility to prey.Close similarity between male and red female weight gain ratesrelative to unmanipulated females suggests that red spots mayalso be a hunting handicap for males. [Behav Ecol 7: 465–473(1996)]     

Linking the evolution and form of warning coloration in nature

Many animals are toxic or unpalatable and signal this to predators with warning signals (aposematism). Aposematic appearance has long been a classical system to study predator–prey interactions, communication and signalling, and animal behaviour and learning. The area has received considerable empirical and theoretical investigation. However, most research has centred on understanding the initial evolution of aposematism, despite the fact that these studies often tell us little about the form and diversity of real warning signals in nature. In contrast, less attention has been given to the mechanistic basis of aposematic markings; that is, ‘what makes an effective warning signal?’, and the efficacy of warning signals has been neglected. Furthermore, unlike other areas of adaptive coloration research (such as camouflage and mate choice), studies of warning coloration have often been slow to address predator vision and psychology. Here, we review the current understanding of warning signal form, with an aim to comprehend the diversity of warning signals in nature. We present hypotheses and suggestions for future work regarding our current understanding of several inter-related questions covering the form of warning signals and their relationship with predator vision, learning, and links to broader issues in evolutionary ecology such as mate choice and speciation.     

Palatablility and escaping ability in Neotropical butterflies: tests with wild kingbirds (Tyrannus melancholicus, Tyrannidae)

The palatability and the ability of neotropical butterflies to escape after being detected, attacked and captured by wild kingbirds ( Tyrannus melancholicus Vieillot), was investigated by the release of 668 individuals of 98 butterfly species close to the birds, during their usual feeding activities. Most of the butterflies were attacked and eaten. Only the troidine swallowtails ( Parities and Battus ; Papilionidae) were consistently rejected on taste and elicited aversive behaviours in birds. Most other aposematic and/or mimetic species in the gehera Danaus and Lycorea (Danainae), Dione, Eueides and Heliconius (Heliconiinae), Hypothyris, Mechanitis and Melinaea (Ithomfinae), Biblis, Callicore and Diaethria (Limenitidinae) were generally eaten. Cryptic and non-mimetic species were always attacked and, if captured, they were also eaten. All Apaturinae, Charaxinae, Nymphalinae, Hesperidae, most Limenitidinae, Heliconiinag ( Agraulis, Dryas, Dryadula and Philaethria ) and Papilionidae ( Eurytides, Heraclides and Protesilaus ) were in this group. Results indicate that the learning process in kingbirds may demand a large mortality in prey populations, even among species generally accepted as unpalatable and aposematic. They also support the assertion that escaping ability and unpalatability evolved in butterflies as alternative strategies to avoid predation by birds. Mimetic relationships among several species are discussed. Evidence for the evolution of aposematism not related to unpalatability, but to escaping ability, was found for two hard-to-catch Morpho species.     

Great tits (Parus major) searching for artificial prey: implications for cryptic coloration and symmetry

It has been suggested that bilateral symmetry may impose a costfor animals relying on camouflage because symmetric color patternsmight increase the risk of detection. We tested the effect ofsymmetry on crypsis, carrying out a predation experiment withgreat tits (Parus major) and black-and-white–patterned,artificial prey items and background. First, we found that detectiontime was significantly longer for a highly cryptic, asymmetricpattern based on a random sample of the background than forits symmetric variants. Second, we were able to arrange theelements of a prey pattern in a way that the resulting asymmetricpattern was highly cryptic and, furthermore, its symmetric variantwas highly cryptic as well. We conclude that symmetry may imposea substantial cost on cryptic patterns, but this cost variesamong patterns. This suggests that for prey, which predatorstypically view from an angle exposing their symmetry, selectionfor pattern asymmetry may be less important and selection fordecreased detectability cost of symmetry may be more importantthan previously thought. This may help to understand the existenceof so many prey with cryptic, symmetric color patterns.     

Fearful symmetry: pattern size and asymmetry affects aposematic signal efficacy

Aposematic animals use anti-predator defence mechanisms such as distastefulness coupled with distinctive odours, sounds, or colour visual signals to predation from domestic chicks we show that the protective value of such visual warning displays is enhanced by increasing size of the signal pattern elements and decreased by pattern asymmetry. These results provide the first experimental evidence that predation may select for individual symmetry of visual warning displays, and concur with earlier demonstrations that asymmetric signals are more difficult to detect, learn, and remember, compared to symmetric signals. Collectively, our findings suggest that prey species possessing warning coloration should be subjected to selection for large and symmetric pattern elements. This revised version was published online in July 2006 with corrections to the Cover Date.     

The protective value of conspicuous signals is not impaired by shape, size, or position asymmetry

Various conspicuous signals in nature promote initial and learnedavoidance by predators. It is widely thought that such signalsare most effective when highly symmetrical in features suchas size and shape, supported by recent laboratory experimentswith domestic chicks and artificial prey. However, no studyhas investigated the effect of asymmetry on conspicuous signalsin a natural setting, where viewing distances, angles, predatorspecies, and light conditions vary and where predators encounterprey sequentially rather than simultaneously. We undertook 2field experiments with artificial gray-scale prey, marked witha pair of white markings presented to wild avian predators,to test the effect of asymmetry on the survival value of conspicuoussignals in the field. Experiment 1 had treatments with symmetricalspots or with spots asymmetrical in area between 5 and 50%.All marked treatments survived better than unmarked controls,but there was no benefit of being symmetrical. Experiment 2tested the effect of possessing markings asymmetrical for shapeor position and any additive effect of these 2 features. Again,symmetry conferred no benefit and targets with markings asymmetricalfor position and/or shape survived equally well as those withsymmetrical arrangements. These findings indicate that asymmetryin warning signals may not be costly to prey in nature or beof less importance compared with other features of the signal,such as color and overall size.     

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.