Prey body size mediates the predation risk associated with being "odd"

Despite selection pressures on prey animals to maintain phenotypically homogeneous groups, variation in phenotype within animal groups is commonly observed. Although many prey animals preferentially associate with size-matched individuals, a lack of preference or a preference for nonmatching group mates is also commonly observed. We suggest that the assortative response to predation risk may be mediated by body size because larger bodied prey may be at greater risk of predation than smaller bodied prey when in a mixed group due to their greater potential profitability. We test this idea by observing attacks by three-spine sticklebacks Gasterosteus aculeatus on mixed groups of large and small Daphnia magna prey. We find that smaller Daphnia are at greatest risk when they form the majority of the group, whereas larger Daphnia are at the greatest predation risk when they form the minority. Thus, we predict that both large and small prey should benefit by association with large prey, generating a potential conflict over group membership that may lead to the mixed phenotype groups we observe in nature

Conflict between background matching and social signalling in a colour-changing freshwater fish

The ability to change coloration allows animals to modify their patterning to suit a specific function. Many freshwater fishes, for example, can appear cryptic by altering the dispersion of melanin pigment in the skin to match the visual background. However, melanin-based pigments are also used to signal dominance among competing males; thus colour change for background matching may conflict with colour change for social status signalling. We used a colour-changing freshwater fish to investigate whether colour change for background matching influenced aggressive interactions between rival males. Subordinate males that had recently darkened their skin for background matching received heightened aggression from dominant males, relative to males whose coloration had not changed. We then determined whether the social status of a rival male, the focal male's previous social status, and his previous skin coloration, affected a male's ability to change colour for background matching. Social status influenced skin darkening in the first social encounter, with dominant males darkening more than subordinate males, but there was no effect of social status on colour change in the second social encounter. We also found that the extent of skin colour change (by both dominant and subordinate males) was dependent on previous skin coloration, with dark males displaying a smaller change in coloration than pale males. Our findings suggest that skin darkening for background matching imposes a significant social cost on subordinate males in terms of increased aggression. We also suggest that the use of melanin-based signals during social encounters can impede subsequent changes in skin coloration for other functions, such as skin darkening for background matching

Colour change and assortment in the western rainbowfish

Grouping behaviour is widespread across the animal kingdom, and is known to reduce an individual's risk of predation, for example through predator confusion. Theory predicts that individuals that are different in appearance to the rest of the group are at a greater risk of predation because they are more conspicuous to predators (the ‘oddity’ effect). Thus, animals should choose group mates that are the most similar in appearance to themselves. Another common antipredator tactic is crypsis (camouflage). Fishes are capable of changing colour to match their visual background, but few studies have examined how this might influence shoaling decisions, particularly in the context of the oddity effect. We induced colour pattern changes in a colourful species of freshwater fish, the western rainbowfish, Melanotaenia australis, by maintaining fish in dark and pale aquaria for 2 weeks. Analysis of the proportion of black body pigmentation confirmed that rainbowfish in dark environments developed darker colour patterns than those held in pale environments. We then conducted behavioural observations to determine whether fish subsequently based their shoaling decisions on body coloration. We found that rainbowfish preferred to shoal with similar individuals; fish that had been held in dark aquaria preferred to shoal with other dark fish and fish from pale aquaria preferred other pale fish. Our findings are consistent with the predictions of the oddity effect and demonstrate how morphological colour pattern changes and behavioural decisions interact to mediate antipredator tactics in fish

Costs of colour change in fish: food intake and behavioural decisions

Many animals, particularly reptiles, amphibians, fish and cephalopods, have the ability to change their body colour, for functions including thermoregulation, signalling and predator avoidance. Many fish plastically darken their body colouration in response to dark visual backgrounds, and this functions to reduce predation risk. Here, we tested the hypotheses that colour change in fish (1) carries with it an energetic cost and (2) affects subsequent shoal and habitat choice decisions. We demonstrate that guppies (Poecilia reticulata) change colour in response to dark and light visual backgrounds, and that doing so carries an energetic cost in terms of food consumption. By increasing food intake, however, guppies are able to maintain growth rates and meet the energetic costs of changing colour. Following colour change, fish preferentially choose habitats and shoals that match their own body colouration, and maximise crypsis, thus avoiding the need for further colour change but also potentially paying an opportunity cost associated with restriction to particular habitats and social associates. Thus, colour change to match the background is complemented by behavioural strategies, which should act to maximise fitness in variable environments. © 2013. Published by The Company of Biologists Ltd

Mixed-phenotype grouping: the interaction between oddity and crypsis

Aggregations of different-looking animals are frequently seen in nature, despite well-documented selection pressures on individuals to maintain phenotypically homogenous groups. Two well-known theories, the ‘confusion effect’ (reduced ability of a predator to accurately target an individual in a group) and the ‘oddity effect’ (preferential targeting of phenotypically distinct, ‘odd’, individuals) act together to predict the evolution of behaviours in prey that lead to groups of animals that are homogeneous in appearance. In contrast, a recently proposed mechanism suggests that mixed groups could be maintained if one species in a mixed group is more conspicuous against the habitat than the other, as confusion effects generated by the conspicuous species impede predator targeting of the cryptic species; thus, cryptic species benefit from association with conspicuous ones. We test these contrasting predictions from the perspective of both predators and prey, and show that cryptic individual Daphnia are at reduced risk of predation from three-spine sticklebacks Gasterosteus aculeatus when in mixed-phenotype groups, a risk that is reduced further as the number of conspicuous individuals increases, supporting the hypothesis for the evolution of mixed groups. In contrast, while the preference for associating with colour-matched conspecifics by mollies (Poecilia sphenops) was reduced when they were cryptic, we found no evidence for active association with conspicuous conspecifics. We conclude that prey animals must balance the relative risks of oddity and conspicuousness in their social decisions, and that this could potentially lead to the evolution of mixed-phenotype grouping as a response to predation risk alone

Balancing the dilution and oddity effects: Decisions depend on body size

Background Grouping behaviour, common across the animal kingdom, is known to reduce an individual's risk of predation; particularly through dilution of individual risk and predator confusion (predator inability to single out an individual for attack). Theory predicts greater risk of predation to individuals more conspicuous to predators by difference in appearance from the group (the ‘oddity’ effect). Thus, animals should choose group mates close in appearance to themselves (eg. similar size), whilst also choosing a large group. Methodology and Principal Findings We used the Trinidadian guppy (Poecilia reticulata), a well known model species of group-living freshwater fish, in a series of binary choice trials investigating the outcome of conflict between preferences for large and phenotypically matched groups along a predation risk gradient. We found body-size dependent differences in the resultant social decisions. Large fish preferred shoaling with size-matched individuals, while small fish demonstrated no preference. There was a trend towards reduced preferences for the matched shoal under increased predation risk. Small fish were more active than large fish, moving between shoals more frequently. Activity levels increased as predation risk decreased. We found no effect of unmatched shoal size on preferences or activity. Conclusions and Significance Our results suggest that predation risk and individual body size act together to influence shoaling decisions. Oddity was more important for large than small fish, reducing in importance at higher predation risks. Dilution was potentially of limited importance at these shoal sizes. Activity levels may relate to how much sampling of each shoal was needed by the test fish during decision making. Predation pressure may select for better decision makers to survive to larger size, or that older, larger fish have learned to make shoaling decisions more efficiently, and this, combined with their size relative to shoal-mates, and attractiveness as prey items influences shoaling decisions

Data from: Conflict between background matching and social signalling in a colour-changing freshwater fish

The ability to change coloration allows animals to modify their patterning to suit a specific function. Many freshwater fishes, for example, can appear cryptic by altering the dispersion of melanin pigment in the skin to match the visual background. However, melanin-based pigments are also used to signal dominance among competing males; thus colour change for background matching may conflict with colour change for social status signalling. We used a colour-changing freshwater fish to investigate whether colour change for background matching influenced aggressive interactions between rival males. Subordinate males that had recently darkened their skin for background matching received heightened aggression from dominant males, relative to males whose coloration had not changed. We then determined whether the social status of a rival male, the focal male's previous social status, and his previous skin coloration, affected a male's ability to change colour for background matching. Social status influenced skin darkening in the first social encounter, with dominant males darkening more than subordinate males, but there was no effect of social status on colour change in the second social encounter. We also found that the extent of skin colour change (by both dominant and subordinate males) was dependent on previous skin coloration, with dark males displaying a smaller change in coloration than pale males. Our findings suggest that skin darkening for background matching imposes a significant social cost on subordinate males in terms of increased aggression. We also suggest that the use of melanin-based signals during social encounters can impede subsequent changes in skin coloration for other functions, such as skin darkening for background matching

Experiment 1 - male-female interactions

Counts of interactions directed from both dominant and subordinate male towards the female in experiment

Experiment 1 - body size

Body size of the fish in experiment 1 as described in the manuscript, in mm

Experiment 2 - colour change

Details of percentage black body colouration before and after each interaction in experiment