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Social transmission of avoidance among predators facilitates the spread of novel prey

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https://doi.org/10.1038/s41559-017-0418-x
1Department of Zoology, University of Cambridge, Cambridge, UK. 2Helsinki Institute of Life Science & Department of Biosciences, University of Helsinki,
Helsinki, Finland. 3Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland. 4Centre of Excellence in
Biological Interactions, University of Jyväskylä, Jyväskylä, Finland. *e-mail: rt303@cam.ac.uk
Since the first description of aposematism over 150 years ago1,
explaining how these conspicuous warning signals evolve to
protect prey in the face of hungry predators remains a chal-
lenge24. Aposematic displays confer little advantage until preda-
tor populations associate the prey’s display with its unprofitability,
and while conspicuous signals are easy to detect and facilitate rapid
learning5, this feature also means they are often taken much more
readily than cryptic prey during predator education5,6. If all preda-
tors must consume novel conspicuous prey to learn, then apose-
matism is unlikely to evolve2, and it cannot be maintained easily
if immigrants or juvenile predators are naïve7,8. This becomes par-
ticularly problematic when prey are lethal, as predators have no
opportunity to learn from their foraging mistakes9. Nevertheless,
aposematism is a widespread defence with multiple evolutionary
origins, showing that it can establish across diverse predator–prey
systems10,11.
Many factors might assist aposematic phenotypes in overcom-
ing this cost of conspicuousness to reach fixation in prey popula-
tions11, although experiments in the laboratory and field suggest the
puzzle is yet to be fully resolved4. For example, aggregating reduces
attack rates endured by unpalatable prey12, but predators still require
repeated encounters with prey aggregations to learn avoidance12,
and aposematic displays are more common among non-aggregating
prey3. Wariness of novel food items may confer an initial advan-
tage for aposematic prey11. However, experiments demonstrate that
dietary conservatism is rarely sufficient to reduce the initial preda-
tion risk below that of cryptic phenotypes13, and social effects dur-
ing foraging encourage predators to become less conservative about
incorporating novel foods into their diet14. Even innate biases against
common warning signals (for example, black and yellow stripes) are
insufficient to protect novel prey completely: novel aposemes suffer
higher mortality overall than cryptic phenotypes13, perhaps because
reinforcement is required for predators’ initial biases to become
avoidance15, and juvenile predators can show less aversion to novel
prey than adults7,15. Furthermore, when a predator’s nutritional state
declines, it increases its consumption of unpalatable prey4, meaning
that aposematic prey in the wild continue to face predation8, even
when some of the population is educated16.
Considering the information ecology of aposematism17 may help
reconcile how it evolves and persists. When encountering novel
prey, predators face uncertainty about its palatability and nutritional
benefit4 so, in theory, they should acquire as much information as
possible before risking consumption17,18. Previous work has focused
on predators becoming educated about warning signals through
interacting with and consuming prey themselves4 (that is, personal
information), perhaps influenced by innate preferences and biases
against colours or patterns15, or wariness of unusual foods in gen-
eral11. However, paying attention to the foraging behaviour of oth-
ers (that is, social information17) could provide an additional potent
source of information19. Social transmission of food aversions has
been demonstrated in a range of taxa: for example, vervet monkeys
learn to prefer palatable rather than unpalatable foods by observing
educated troop members20, juvenile great tits increase their avoid-
ance of aposematic prey if they observe an adult eat an alternative21,
and tamarin monkeys22, red-winged blackbirds23, house sparrows24
and domestic chicks25 avoid foods after observing a conspecific
show distress. Observing another’s characteristic response to dis-
tasteful food can also increase chickens’ wariness of two typical
colours used by aposematic prey26. However, whether social trans-
mission facilitates the evolution and spread of novel conspicuous
prey compared with an alternative phenotype27 remains untested.
Here we combine experiments with a mathematical model to test
whether social transmission of avoidance among predators enables
novel aposematic prey phenotypes to reach fixation more readily
than was previously assumed. We used the novel-world method5,28
where naïve predators search in an artificial landscape for artificial
prey (paper packets containing food) marked with novel signals
that are either cryptic (they share the signal printed on the land-
scape) or conspicuous5,28. The palatability of prey is manipulated
by soaking small pieces of almond in chloroquinephosphate—a
mild toxin that facilitates associative learning29. This method avoids
using signals that are found in a predator’s current environment or
Social transmission of avoidance among predators
facilitates the spread of novel prey
Rose Thorogood 1,2*, Hanna Kokko3 and Johanna Mappes4
Warning signals are an effective defence strategy for aposematic prey, but only if they are recognized by potential predators.
If predators must eat prey to associate novel warning signals with unpalatability, how can aposematic prey ever evolve? Using
experiments with great tits (Parus major) as predators, we show that social transmission enhances the acquisition of avoid-
ance by a predator population. Observing another predator’s disgust towards tasting one novel conspicuous prey item led to
fewer aposematic than cryptic prey being eaten for the predator population to learn. Despite reduced personal encounters with
unpalatable prey, avoidance persisted and increased over subsequent trials. Next we use a mathematical model to show that
social transmission can shift the evolutionary trajectory of prey populations from fixation of crypsis to fixation of aposematism
more easily than was previously thought. Therefore, social information use by predators has the potential to have evolutionary
consequences across ecological communities.
NATURE ECOLOGY & EVOLUTION | VOL 2 | FEBRUARY 2018 | 254–261 | www.nature.com/natecolevol
254

Supplementary resource (1)

... 2 information can shape social structures and determine how individuals interact with each other and the wider environment (Cantor et al. 2021). Social transmission, therefore, has the potential to relax or intensify selection, or generate novel selection pressures, including during species interactions (Thorogood andDavies 2012, Whitehead et al. 2019). Although considering social information use can help answer open questions about species coevolution and community dynamics (Thorogood and Davies 2012, Gil et al. 2018, Whitehead et al. 2019, there has been little synthesis evaluating how social information use can influence ecological and evolutionary dynamics within the context of species interactions (Cantor et al. 2021). ...
... Since then, there has been extensive research into how prey can use social information to avoid predators (reviewed in Brown 2003, Griffin 2004, Ferrari et al. 2010, Magrath et al. 2015, but there is also a growing set of studies on social behaviour of predators. Indeed, recent work suggests that social information transfer among predators can affect the frequency-dependent dynamics of prey defences, and resolve long-standing questions in evolutionary biology, such as the maintenance of aposematism (Thorogood et al. 2018). However, we still know little about these populationand community-level effects (Gil et al. 2018). ...
... Aposematic prey are therefore expected to suffer high predation from naïve predators, which makes the evolution and maintenance of aposematism paradoxical (Fisher 1930, Guilford 1988, Alatalo and Mappes 1996, Mappes et al. 2014. Social learning about prey defences provides one answer to this evolutionary puzzle because predators require fewer personal encounters with prey to adopt accurate identification (Guilford 1988, Thorogood et al. 2018. Accurate identification by predators also determines the success of mimetic defences. ...
Article
Full-text available
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.
... Birds are common predators of many aposematic species, and often perform beak wiping and head shaking when tasting an unpalatable prey (Clark 1970;Rowland et al. 2015;Hämäläinen et al. 2020a). These visible displays ("distaste responses") can provide observers information about prey unprofitability, and several studies have now demonstrated that avian predators can learn to avoid unpalatable prey by observing negative foraging experiences of both conspecifics (Mason and Reidinger 1982;Johnston et al. 1998; Thorogood et al. 2018;Hämäläinen et al. 2019) and heterospecifics (Mason et al. 1984;Hämäläinen et al. 2020bHämäläinen et al. , 2021a. This allows predators to acquire information about prey unprofitability without the risk of ingesting potentially toxic food (Skelhorn 2011;Thorogood et al. 2018;Brooke et al. 2019;Hämäläinen et al. 2019). ...
... These visible displays ("distaste responses") can provide observers information about prey unprofitability, and several studies have now demonstrated that avian predators can learn to avoid unpalatable prey by observing negative foraging experiences of both conspecifics (Mason and Reidinger 1982;Johnston et al. 1998; Thorogood et al. 2018;Hämäläinen et al. 2019) and heterospecifics (Mason et al. 1984;Hämäläinen et al. 2020bHämäläinen et al. , 2021a. This allows predators to acquire information about prey unprofitability without the risk of ingesting potentially toxic food (Skelhorn 2011;Thorogood et al. 2018;Brooke et al. 2019;Hämäläinen et al. 2019). However, in these studies, predators observed very strong cues, such as demonstrators vomiting (Mason and Reidinger 1982;Mason et al. 1984) or performing intensive head shaking and beak wiping after eating the prey (Thorogood et al. 2018;Hämäläinen et al. 2019Hämäläinen et al. , 2020b, and we do not know how common these strong responses are in a wild predator population, and whether predators respond to weaker cues about prey defenses. ...
... This allows predators to acquire information about prey unprofitability without the risk of ingesting potentially toxic food (Skelhorn 2011;Thorogood et al. 2018;Brooke et al. 2019;Hämäläinen et al. 2019). However, in these studies, predators observed very strong cues, such as demonstrators vomiting (Mason and Reidinger 1982;Mason et al. 1984) or performing intensive head shaking and beak wiping after eating the prey (Thorogood et al. 2018;Hämäläinen et al. 2019Hämäläinen et al. , 2020b, and we do not know how common these strong responses are in a wild predator population, and whether predators respond to weaker cues about prey defenses. ...
Article
Animals gather social information by observing the behavior of others, but how the intensity of observed cues influences decision-making is rarely investigated. This is crucial for understanding how social information influences ecological and evolutionary dynamics. For example, observing a predator’s distaste of unpalatable prey can reduce predation by naïve birds, and help explain the evolution and maintenance of aposematic warning signals. However, previous studies have only used demonstrators that responded vigorously, showing intense beak-wiping after tasting prey. Therefore, here we conducted an experiment with blue tits (Cyanistes caeruleus) informed by variation in predator responses. First, we found that the response to unpalatable food varies greatly, with only few individuals performing intensive beak-wiping. We then tested how the intensity of beak-wiping influences observers’ foraging choices using video-playback of a conspecific tasting a novel conspicuous prey item. Observers were provided social information from 1) no distaste response, 2) a weak distaste response, or 3) a strong distaste response, and were then allowed to forage on evolutionarily novel (artificial) prey. Consistent with previous studies, we found that birds consumed fewer aposematic prey after seeing a strong distaste response, however, a weak response did not influence foraging choices. Our results suggest that while beak-wiping is a salient cue, its information content may vary with cue intensity. Furthermore, the number of potential demonstrators in the predator population might be lower than previously thought, although determining how this influences social transmission of avoidance in the wild will require uncovering the effects of intermediate cue salience.
... There is evidence for their social 81 transmission in several systems (Hämäläinen et al. in press). These include humpback whales using a 82 novel lobtail feeding technique (Allen et al. 2013), and wild populations of birds learning about novel 83 prey phenotypes, where they are predicted to impact prey evolution (Thorogood et al. 2018). 84 ...
... response to social learning to avoid dangerous or toxic prey (other than the focal prey modeled here) 253 (e.g. Thorogood et al. 2018). Under the assumption that m 2 < m 1 , dropping other subscripts, one 254 condition for stability is that ...
Preprint
Individual behavioral variation is common, yet often we do not know how it is maintained. A potential explanation is that some behaviors must be acquired rather than genetically inherited. We investigate the social transmission of behavioral innovations, which can be key for the success of predator species, especially in contexts where environmental changes take place. We examine innovation in two classic predator-prey models. We assume that innovations increase predator attack rates or conversion efficiencies, or that innovations reduce predator mortality or prey handling time. We find that a common outcome of innovations is the destabilization of the system. Destabilizing effects include increasing oscillations or limit cycles. If either of these outcomes increases the risk of extinction, innovations that benefit individual predators may not have positive long-term effects on predator populations. Furthermore, as populations cycle, innovative individuals can be nearly eliminated, maintaining temporal behavioral variability. The destabilizing effects of behavioral innovations on predator-prey dynamics could have implications for biological invasions, urban populations, endangered species, and, more broadly, the maintenance of behavioral polymorphisms.
... Dissecting behaviour is innate in some mustelids [78,117,118], and in some birds this behaviour is thought to be exapted from fruit-eating, and would therefore be of low cost to maintain given its benefit in other contexts [17,92]. Dissecting behaviour may evolve and be maintained via cultural transfer [105] because headshaking in response to aversive stimuli could be used by conspecifics to guide dissecting behaviour [119], and for individuals to develop discriminatory chemosensory behaviour [17]. The widespread occurrence of dissecting behaviour suggests a shared ability to taste and avoid CTS in predators [120]. ...
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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.
... The effectiveness of disruptive and aversive management techniques rely on behavioural responses from animals. One of the potential advantages of these techniques over lethal methods is that individuals have the opportunity to learn and persist in the environment where they can maintain ecological functions, compete with conspecifics, and in some cases pass on knowledge of cues to other individuals (Thorogood et al. 2018). For these reasons, understanding the cognitive processes that underlie the desired response, including perception, learning and decision-making, makes it possible to design interventions where only a few unpleasant exposures are needed, which minimises harm to realise long-term behavioural change (Greggor et al. 2014). ...
Chapter
This chapter provides general operating procedures (GOPs) and guidelines for a variety of non-lethal techniques, which seek to interrupt, reduce or modify the behaviour of wildlife to decrease the occurrence of ‘unwanted’or ‘undesirable’behaviours. In Australia such methods are mostly employed for threatened species protection as part of introduced predator management, and for protecting agricultural interests from wildlife (eg to keep carnivores from attacking livestock, or kangaroos from accessing grazing land). However, non-lethal techniques as described in this chapter can be applied to a multitude of management and research contexts (eg to protect humans from shark attack). Methods covered include guardian animals, disruptive stimuli (frightening devices, lights, sounds), conditioned taste aversion (odours and chemicals) and electric deterrents (fences, shields, collars). These guidelines are written to be complementary to each other given the overlap in many themes that exist across the techniques. A great deal of the literature referred to is drawn from international sources where many of the problems, solutions and ethical implications are similar.
... These findings may have crucial implications in many theoretical and applied ecological contexts, ranging from the invasive dynamics of predator-prey systems to the efficiency of biological control practices. For instance, the recognition of novel predators by naïve prey has been associated with social information use via different perception modalities in group-living fish (Ferrari et al. 2005;Manassa et al. 2013), and similar utilisation of social cues in social birds has been shown to facilitate the spread of novel aposematic prey (Thorogood et al. 2018;Hämäläinen et al. 2021a, b). Such social information-mediated interactions between prey and predators might be more prevalent in natural ecosystems that include non-grouping species as well, contributing to deviations from the predictions of theoretical models in the dynamics of trophic interactions (Polis et al. 2000). ...
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... There is a rich literature on the culture of inherited behaviors across a wide range of taxa emphasizing its evolutionary significance and adaptive importance. This literature includes: song dialects in white-crowned sparrows (Zonotrichia leucophrys) (Marler & Tamura, 1964), foraging sites in birds (Slagsvold & Wiebe, 2011), whale songs (Noad et al., 2000), bottlenose dolphin (Tursiops spp.) foraging traditions (Mann & Sargeant, 2003), humpback whale (Megaptera novaeangliae) feeding methods (Allen et al., 2013), capuchin monkey (Cebus spp.) tool use (Ottoni et al., 2005), sperm whale (Physeter macrocephalus) dialects (Weilgart & Whitehead, 1997), killer whale (Orcinus orca) ecotype evolution (Foote et al., 2016), killer whale diets, foraging strategies, and social conventions (Boran & Heimlich, 1999;Rendell & Whitehead, 2001), ungulate migration (Jesmer et al., 2018), and social transmission of prey avoidance between predators (Thorogood et al., 2018). ...
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... A conditioned aversion to repellent baits may be socially learnt in kea, as in other species. For example, great tits and red-winged blackbirds can socially learn the appetitive value of prey items by observing conspecifics' reactions to eating them [54][55][56]. While studies on kea social learning have focused on the transmission of problem-solving strategies rather than foraging information [48,57,58], determining whether kea socially learn about food preferences would be useful for understanding how best to promote learned aversions in wild populations and so should be a focus of future research. ...
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