Publications by category
Journal articles
Troscianko J, Briolat ES, Gaston KJ, Bennie J, Rosenfeld EJ (In Press). Artificial nighttime lighting impacts visual ecology links between flowers, pollinators and predators. Nature Communications
Hughes A, Briolat E, Arenas L, Liggins E, Stevens M (In Press). Varying benefits of generalist and specialist camouflage in two versus four background environments. Behavioral Ecology
Kikuchi DW, Allen WL, Arbuckle K, Aubier TG, Briolat ES, Burdfield‐Steel ER, Cheney KL, Daňková K, Elias M, Hämäläinen L, et al (2023). The evolution and ecology of multiple antipredator defences.
Journal of Evolutionary Biology,
36(7), 975-991.
Abstract:
The evolution and ecology of multiple antipredator defences
AbstractPrey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g. visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade‐offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.
Abstract.
Yorzinski JL, Troscianko J, Briolat E, Schapiro SJ, Whitham W (2022). A songbird can detect the eyes of conspecifics under daylight and artificial nighttime lighting. Environmental Pollution, 313, 120000-120000.
Briolat ES, Arenas LM, Hughes AE, Liggins E, Stevens M (2021). Generalist camouflage can be more successful than microhabitat specialisation in natural environments.
BMC Ecol Evol,
21(1).
Abstract:
Generalist camouflage can be more successful than microhabitat specialisation in natural environments.
BACKGROUND: Crypsis by background-matching is a critical form of anti-predator defence for animals exposed to visual predators, but achieving effective camouflage in patchy and variable natural environments is not straightforward. To cope with heterogeneous backgrounds, animals could either specialise on particular microhabitat patches, appearing cryptic in some areas but mismatching others, or adopt a compromise strategy, providing partial matching across different patch types. Existing studies have tested the effectiveness of compromise strategies in only a limited set of circumstances, primarily with small targets varying in pattern, and usually in screen-based tasks. Here, we measured the detection risk associated with different background-matching strategies for relatively large targets, with human observers searching for them in natural scenes, and focusing on colour. Model prey were designed to either 'specialise' on the colour of common microhabitat patches, or 'generalise' by matching the average colour of the whole visual scenes. RESULTS: in both the field and an equivalent online computer-based search task, targets adopting the generalist strategy were more successful in evading detection than those matching microhabitat patches. This advantage occurred because, across all possible locations in these experiments, targets were typically viewed against a patchwork of different microhabitat areas; the putatively generalist targets were thus more similar on average to their various immediate surroundings than were the specialists. CONCLUSIONS: Demonstrating close agreement between the results of field and online search experiments provides useful validation of online citizen science methods commonly used to test principles of camouflage, at least for human observers. In finding a survival benefit to matching the average colour of the visual scenes in our chosen environment, our results highlight the importance of relative scales in determining optimal camouflage strategies, and suggest how compromise coloration can succeed in nature.
Abstract.
Author URL.
Caro T, Argueta Y, Briolat ES, Bruggink J, Kasprowsky M, Lake J, Mitchell MJ, Richardson S, How M (2019). Benefits of zebra stripes: Behaviour of tabanid flies around zebras and horses.
PLoS ONE,
14(2).
Abstract:
Benefits of zebra stripes: Behaviour of tabanid flies around zebras and horses
Averting attack by biting flies is increasingly regarded as the evolutionary driver of zebra stripes, although the precise mechanism by which stripes ameliorate attack by ectoparasites is unknown. We examined the behaviour of tabanids (horse flies) in the vicinity of captive plains zebras and uniformly coloured domestic horses living on a horse farm in Britain. Observations showed that fewer tabanids landed on zebras than on horses per unit time, although rates of tabanid circling around or briefly touching zebra and horse pelage did not differ. In an experiment in which horses sequentially wore cloth coats of different colours, those wearing a striped pattern suffered far lower rates of tabanid touching and landing on coats than the same horses wearing black or white, yet there were no differences in attack rates to their naked heads. In separate, detailed video analyses, tabanids approached zebras faster and failed to decelerate before contacting zebras, and proportionately more tabanids simply touched rather than landed on zebra pelage in comparison to horses. Taken together, these findings indicate that, up close, striped surfaces prevented flies from making a controlled landing but did not influence tabanid behaviour at a distance. To counteract flies, zebras swished their tails and ran away from fly nuisance whereas horses showed higher rates of skin twitching. As a consequence of zebras’ striping, very few tabanids successfully landed on zebras and, as a result of zebras’ changeable behaviour, few stayed a long time, or probed for blood.
Abstract.
Briolat E, Zagrobelny M, Olsen C, Blount J, Stevens M (2019). No evidence of quantitative signal honesty across species of aposematic burnet moths (Lepidoptera: Zygaenidae). Journal of Evolutionary Biology, 32, 31-48.
Briolat E, Burdfield-Steel E, Paul S, Rönkä K, Seymoure B, Stankowich T, Stuckert A (2018). Diversity in warning coloration: selective paradox or the norm?.
Biological ReviewsAbstract:
Diversity in warning coloration: selective paradox or the norm?
Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency‐dependent learning. However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population. Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals. Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal. The mechanisms producing warning coloration are also important. Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation. Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator–prey interactions. Predator variability in a range of factors (e.g. perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated. With complex selection regimes at work, polytypisms and polymorphisms may even occur in Müllerian mimicry systems. Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures. Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore. As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species. Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research. A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once‐paradoxical phenomenon, yields a new perspective for the field of aposematic signalling.
Abstract.
Briolat E, Zagrobelny M, Olsen, CE, Blount J, Stevens M (2018). Sex differences but no evidence of quantitative honesty in the warning signals of six-spot burnet moths (Zygaena filipendulae L.). Evolution, 77, 1460-1474.
Publications by year
In Press
Troscianko J, Briolat ES, Gaston KJ, Bennie J, Rosenfeld EJ (In Press). Artificial nighttime lighting impacts visual ecology links between flowers, pollinators and predators. Nature Communications
Hughes A, Briolat E, Arenas L, Liggins E, Stevens M (In Press). Varying benefits of generalist and specialist camouflage in two versus four background environments. Behavioral Ecology
2023
Briolat ES, Hancock GRA, Troscianko J (2023). Adapting genetic algorithms for artificial evolution of visual patterns under selection from wild predators.
Abstract:
Adapting genetic algorithms for artificial evolution of visual patterns under selection from wild predators
Camouflage is a widespread and well-studied anti-predator strategy, yet identifying which patterns provide optimal protection in any given scenario remains challenging. Besides the virtually limitless combinations of colours and patterns available to prey, selection for camouflage strategies will depend on complex interactions between prey appearance, background properties and predator traits, across repeated encounters between co-evolving predators and prey. Experiments in artificial evolution, pairing psychophysics detection tasks with genetic algorithms, offer a promising way to tackle this complexity, but sophisticated genetic algorithms have so far been restricted to screen-based experiments. Here, we present methods to test the evolution of colour patterns on physical prey items, under selection from wild predators in the field. Our techniques expand on a recently-developed open-access pattern generation and genetic algorithm framework, modified to operate alongside artificial predation experiments. In this system, predators freely interact with prey, and the order of attack determines the survival and reproduction of prey patterns into future generations. We demonstrate the feasibility of these methods with a case study, in which free-flying birds feed on artificial prey deployed in semi-natural conditions, against backgrounds differing in three-dimensional complexity. Wild predators reliably participated in this experiment, foraging for 11 to 16 generations of artificial prey and encountering a total of 1,296 evolved prey items. Changes in prey pattern across generations indicated improvements in several metrics of similarity to the background, and greater edge disruption, although effect sizes were relatively small. Computer-based replicates of these trials, with human volunteers, highlighted the importance of starting population parameters for subsequent evolution, a key consideration when applying these methods. Ultimately, these methods provide pathways for integrating complex genetic algorithms into more naturalistic predation trials. Customisable open-access tools should facilitate application of these tools to investigate a wide range of visual pattern types in more ecologically-relevant contexts.
Abstract.
Kikuchi DW, Allen WL, Arbuckle K, Aubier TG, Briolat ES, Burdfield‐Steel ER, Cheney KL, Daňková K, Elias M, Hämäläinen L, et al (2023). The evolution and ecology of multiple antipredator defences.
Journal of Evolutionary Biology,
36(7), 975-991.
Abstract:
The evolution and ecology of multiple antipredator defences
AbstractPrey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g. visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade‐offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.
Abstract.
2022
Yorzinski JL, Troscianko J, Briolat E, Schapiro SJ, Whitham W (2022). A songbird can detect the eyes of conspecifics under daylight and artificial nighttime lighting. Environmental Pollution, 313, 120000-120000.
2021
Briolat ES, Arenas LM, Hughes AE, Liggins E, Stevens M (2021). Generalist camouflage can be more successful than microhabitat specialisation in natural environments.
BMC Ecol Evol,
21(1).
Abstract:
Generalist camouflage can be more successful than microhabitat specialisation in natural environments.
BACKGROUND: Crypsis by background-matching is a critical form of anti-predator defence for animals exposed to visual predators, but achieving effective camouflage in patchy and variable natural environments is not straightforward. To cope with heterogeneous backgrounds, animals could either specialise on particular microhabitat patches, appearing cryptic in some areas but mismatching others, or adopt a compromise strategy, providing partial matching across different patch types. Existing studies have tested the effectiveness of compromise strategies in only a limited set of circumstances, primarily with small targets varying in pattern, and usually in screen-based tasks. Here, we measured the detection risk associated with different background-matching strategies for relatively large targets, with human observers searching for them in natural scenes, and focusing on colour. Model prey were designed to either 'specialise' on the colour of common microhabitat patches, or 'generalise' by matching the average colour of the whole visual scenes. RESULTS: in both the field and an equivalent online computer-based search task, targets adopting the generalist strategy were more successful in evading detection than those matching microhabitat patches. This advantage occurred because, across all possible locations in these experiments, targets were typically viewed against a patchwork of different microhabitat areas; the putatively generalist targets were thus more similar on average to their various immediate surroundings than were the specialists. CONCLUSIONS: Demonstrating close agreement between the results of field and online search experiments provides useful validation of online citizen science methods commonly used to test principles of camouflage, at least for human observers. In finding a survival benefit to matching the average colour of the visual scenes in our chosen environment, our results highlight the importance of relative scales in determining optimal camouflage strategies, and suggest how compromise coloration can succeed in nature.
Abstract.
Author URL.
2019
Caro T, Argueta Y, Briolat ES, Bruggink J, Kasprowsky M, Lake J, Mitchell MJ, Richardson S, How M (2019). Benefits of zebra stripes: Behaviour of tabanid flies around zebras and horses.
PLoS ONE,
14(2).
Abstract:
Benefits of zebra stripes: Behaviour of tabanid flies around zebras and horses
Averting attack by biting flies is increasingly regarded as the evolutionary driver of zebra stripes, although the precise mechanism by which stripes ameliorate attack by ectoparasites is unknown. We examined the behaviour of tabanids (horse flies) in the vicinity of captive plains zebras and uniformly coloured domestic horses living on a horse farm in Britain. Observations showed that fewer tabanids landed on zebras than on horses per unit time, although rates of tabanid circling around or briefly touching zebra and horse pelage did not differ. In an experiment in which horses sequentially wore cloth coats of different colours, those wearing a striped pattern suffered far lower rates of tabanid touching and landing on coats than the same horses wearing black or white, yet there were no differences in attack rates to their naked heads. In separate, detailed video analyses, tabanids approached zebras faster and failed to decelerate before contacting zebras, and proportionately more tabanids simply touched rather than landed on zebra pelage in comparison to horses. Taken together, these findings indicate that, up close, striped surfaces prevented flies from making a controlled landing but did not influence tabanid behaviour at a distance. To counteract flies, zebras swished their tails and ran away from fly nuisance whereas horses showed higher rates of skin twitching. As a consequence of zebras’ striping, very few tabanids successfully landed on zebras and, as a result of zebras’ changeable behaviour, few stayed a long time, or probed for blood.
Abstract.
Briolat E, Zagrobelny M, Olsen C, Blount J, Stevens M (2019). No evidence of quantitative signal honesty across species of aposematic burnet moths (Lepidoptera: Zygaenidae). Journal of Evolutionary Biology, 32, 31-48.
2018
Briolat E, Burdfield-Steel E, Paul S, Rönkä K, Seymoure B, Stankowich T, Stuckert A (2018). Diversity in warning coloration: selective paradox or the norm?.
Biological ReviewsAbstract:
Diversity in warning coloration: selective paradox or the norm?
Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency‐dependent learning. However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population. Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals. Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal. The mechanisms producing warning coloration are also important. Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation. Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator–prey interactions. Predator variability in a range of factors (e.g. perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated. With complex selection regimes at work, polytypisms and polymorphisms may even occur in Müllerian mimicry systems. Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures. Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore. As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species. Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research. A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once‐paradoxical phenomenon, yields a new perspective for the field of aposematic signalling.
Abstract.
Briolat E, Zagrobelny M, Olsen, CE, Blount J, Stevens M (2018). Sex differences but no evidence of quantitative honesty in the warning signals of six-spot burnet moths (Zygaena filipendulae L.). Evolution, 77, 1460-1474.