Social information use by predators : expanding the information ecology of prey defences

Social information use is well documented across the animal kingdom, but how it influences ecological and evolutionary processes is only just beginning to be investigated. Here we evaluate how social transmission may influence species interactions and potentially change or create novel selection pressures by focusing on predator-prey interactions, one of the best studied examples of species coevolution. There is extensive research into how prey can use social information to avoid predators, but little synthesis of how social transmission among predators can influence the outcome of different stages of predation. Here we review evidence that predators use social information during 1) encounter, 2) detection, 3) identification, 4) approach, 5) subjugation and 6) consumption. We use this predation sequence framework to evaluate the implications of social information use on current theoretical predictions about predator-prey dynamics, and find that social transmission has the potential to alter selection pressures for prey defences at each predation stage. This suggests that considering social interactions can help answer open questions about species coevolution, and also predict how populations and communities respond to rapid human-induced changes in the environment.Peer reviewe

Can video playback provide social information for foraging blue tits?

Video playback is becoming a common method for manipulating social stimuli in experiments. Parid tits are one of the most commonly studied groups of wild birds. However, it is not yet clear if tits respond to video playback or how their behavioural responses should be measured. Behaviours may also differ depending on what they observe demonstrators encountering. Here we present blue tits (Cyanistes caeruleus) videos of demonstrators discovering palatable or aversive prey (injected with bitter-tasting Bitrex) from coloured feeding cups. First we quantify variation in demonstrators' responses to the prey items: aversive prey provoked high rates of beak wiping and head shaking. We then show that focal blue tits respond differently to the presence of a demonstrator on a video screen, depending on whether demonstrators discover palatable or aversive prey. Focal birds faced the video screen more during aversive prey presentations, and made more head turns. Regardless of prey type, focal birds also hopped more frequently during the presence of a demonstrator (compared to a control video of a different coloured feeding cup in an empty cage). Finally, we tested if demonstrators' behaviour affected focal birds' food preferences by giving individuals a choice to forage from the same cup as a demonstrator, or from the cup in the control video. We found that only half of the individuals made their choice in accordance to social information in the videos, i.e., their foraging choices were not different from random. Individuals that chose in accordance with a demonstrator, however, made their choice faster than individuals that chose an alternative cup. Together, our results suggest that video playback can provide social cues to blue tits, but individuals vary greatly in how they use this information in their foraging decisions.Peer reviewe

Perch, Perca fluviatilis show a directional preference for, but do not increase attacks toward, prey in response to water-borne cortisol

In freshwater environments, chemosensory cues play an important role in predatorprey interactions. Prey use a variety of chemosensory cues to detect and avoid predators. However, whether predators use the chemical cues released by disturbed or stressed prey has received less attention. Here we tested the hypothesis that the disturbance cue cortisol, in conjunction with visual cues of prey, elevates predatory behavior. We presented predators (perch, Perca fluviatilis) with three chemosensory choice tests and recorded their location, orientation, and aggressive behavior. We compared the responses of predators when provided with (i) visual cues of prey only (two adjacent tanks containing sticklebacks); (ii) visual and natural chemical cues of prey vs. visual cues only; and (iii) visual cues of prey with cortisol vs. visual cues only. Perch spent a significantly higher proportion of time in proximity to prey, and orientated toward prey more, when presented with a cortisol stimulus plus visual cues, relative to presentations of visual and natural chemical cues of prey, or visual cues of prey only. There was a trend that perch directed a higher proportion of predatory behaviors (number of lunges) toward sticklebacks when presented with a cortisol stimulus plus visual cues, relative to the other chemosensory conditions. But they did not show a significant increase in total predatory behavior in response to cortisol. Therefore, it is not clear whether water-borne cortisol, in conjunction with visual cues of prey, affects predatory behavior. Our results provide evidence that cortisol could be a source of public information about prey state and/or disturbance, but further work is required to confirm this

Defence mitigation by predators of chemically defended prey integrated over the predation sequence and across biological levels with a focus on cardiotonic steroids

Predator–prey interactions have long served as models for the investigation of adaptation and fitness in natural environments. Anti-predator defences such as mimicry and camouflage provide some of the best examples of evolution. Predators, in turn, have evolved sensory systems, cognitive abilities and physiological resistance to prey defences. In contrast to prey defences which have been reviewed extensively, the evolution of predator counter-strategies has received less attention. To gain a comprehensive view of how prey defences can influence the evolution of predator counter-strategies, it is essential to investigate how and when selection can operate. In this review we evaluate how predators overcome prey defences during (i) encounter, (ii) detection, (iii) identification, (iv) approach, (v) subjugation, and (vi) consumption. We focus on prey that are protected by cardiotonic steroids (CTS)—defensive compounds that are found in a wide range of taxa, and that have a specific physiological target. In this system, coevolution is well characterized between specialist insect herbivores and their host plants but evidence for coevolution between CTS-defended prey and their predators has received less attention. Using the predation sequence framework, we organize 574 studies reporting predators overcoming CTS defences, integrate these counter-strategies across biological levels of organization, and discuss the costs and benefits of attacking CTS-defended prey. We show that distinct lineages of predators have evolved dissecting behaviour, changes in perception of risk and of taste perception, and target-site insensitivity. We draw attention to biochemical, hormonal and microbiological strategies that have yet to be investigated as predator counter-adaptations to CTS defences. We show that the predation sequence framework will be useful for organizing future studies of chemically mediated systems and coevolution

Colour change of twig-mimicking peppered moth larvae is a continuous reaction norm that increases camouflage against avian predators

Camouflage, and in particular background-matching, is one of the most commonanti-predator strategies observed in nature. Animals can improve their match to thecolour/pattern of their surroundings through background selection, and/or by plasticcolour change. Colour change can occur rapidly (a few seconds), or it may be slow,taking hours to days. Many studies have explored the cues and mechanisms behindrapid colour change, but there is a considerable lack of information about slow colourchange in the context of predation: the cues that initiate it, and the range of phenotypesthat are produced. Here we show that peppered moth (Biston betularia) larvae respondto colour and luminance of the twigs they rest on, and exhibit a continuous reactionnorm of phenotypes. When presented with a heterogeneous environment of mixed twigcolours, individual larvae specialise crypsis towards one colour rather than developingan intermediate colour. Flexible colour change in this species has likely evolved inassociation with wind dispersal and polyphagy, which result in caterpillars settling andfeeding in a diverse range of visual environments. This is the first example of visuallyinduced slow colour change in Lepidoptera that has been objectively quantified andmeasured from the visual perspective of natural predators

Changes in women’s facial skin color over the ovulatory cycle are not detectable by the human visual system

Human ovulation is not advertised, as it is in several primate species, by conspicuous sexual swellings. However, there is increasing evidence that the attractiveness of women’s body odor, voice, and facial appearance peak during the fertile phase of their ovulatory cycle. Cycle effects on facial attractiveness may be underpinned by changes in facial skin color, but it is not clear if skin color varies cyclically in humans or if any changes are detectable. To test these questions we photographed women daily for at least one cycle. Changes in facial skin redness and luminance were then quantified by mapping the digital images to human long, medium, and shortwave visual receptors. We find cyclic variation in skin redness, but not luminance. Redness decreases rapidly after menstrual onset, increases in the days before ovulation, and remains high through the luteal phase. However, we also show that this variation is unlikely to be detectable by the human visual system. We conclude that changes in skin color are not responsible for the effects of the ovulatory cycle on women’s attractiveness

The peppered moth <i>Biston betularia</i>

Hannah Rowland and colleagues introduce the peppered moth whose industrial melanism was an early evidence for evolution

The antipredator benefits of postural camouflage in peppered moth caterpillars.

Funder: Churchill College, University of Cambridge; doi: http://dx.doi.org/10.13039/501100000742Funder: Projekt DEALCamouflage is the most common form of antipredator defense, and is a textbook example of natural selection. How animals' appearances prevent detection or recognition is well studied, but the role of prey behavior has received much less attention. Here we report a series of experiments with twig-mimicking larvae of the American peppered moth Biston betularia that test the long-held view that prey have evolved postures that enhance their camouflage, and establish how food availability and ambient temperature affect these postures. We found that predators took longer to attack larvae that were resting in a twig-like posture than larvae resting flat against a branch. Larvae that were chilled or food restricted (manipulations intended to energetically stress larvae) adopted a less twig-like posture than larvae that were fed ad libitum. Our findings provide clear evidence that animals gain antipredator benefits from postural camouflage, and suggest that benefits may come at an energetic cost that animals are unwilling or unable to pay under some conditions

Social network centrality predicts dietary decisions in a wild bird population

How individuals balance costs and benefits of group living remains central to understanding sociality. In relation to diet, social foraging provides many advantages but also increases competition. Nevertheless, social individuals may offset increased competition by broadening their diet and consuming novel foods. Despite the expected relationships between social behavior and dietary decisions, how sociality shapes individuals’ novel food consumption remains largely untested in natural populations. Here, we use wild great tits to experimentally test how sociality predicts dietary decisions. We show that individuals with more social connections have higher propensity to use novel foods compared to socially peripheral individuals, and this is unrelated to neophobia, observations, and demographic factors. These findings indicate sociable individuals may offset potential costs of competition by foraging more broadly. We discuss how social environments may drive behavioral change in natural populations, and the implications for the causes and consequences of social strategies and dietary decisions

Ontogeny of color development in two green-brown polymorphic grasshopper species.

Many insects, including several orthopterans, undergo dramatic changes in body coloration during ontogeny. This variation is particularly intriguing in gomphocerine grasshoppers, where the green and brown morphs appear to be genetically determined (Schielzeth & Dieker, 2020, BMC Evolutionary Biology, 20, 63; Winter et al., 2021, Heredity, 127, 66). A better understanding of how these color morphs develop during ontogeny can provide valuable insights into the evolution and ecology of such a widespread color polymorphism. Here, we focus on the color development of two green-brown polymorphic species, the club-legged grasshopper Gomphocerus sibiricus and the steppe grasshopper Chorthippus dorsatus. By following the color development of individuals from hatching to adulthood, we found that color morph differences begin to develop during the second nymphal stage, are clearly defined by the third nymphal stage, and remain stable throughout the life of an individual. Interestingly, we also observed that shed skins of late nymphal stages are identifiable by color morphs based on their yellowish coloration, rather than the green that marks green body parts. Furthermore, by assessing how these colors are perceived by different visual systems, we found that certain potential predators can chromatically discriminate between morphs, while others may not. These results suggest that the putative genes controlling color morph are active during the early stages of ontogeny, and that green color is likely composed of two components, one present in the cuticle and one not. In addition, the effectiveness of camouflage appears to vary depending on the specific predator involved