Predator-prey dynamics are an important evolutionary driver of escalating predation mode and efficiency, and commensurate responses of prey [1-3]. Among these strategies, camouflage is important for visual concealment, with countershading the most universally observed [4-6]. Extant terrestrial herbivores free of significant predation pressure, due to large size or isolation, do not exhibit countershading. Modern predator-prey dynamics may not be directly applicable to those of the Mesozoic due to the dominance of very large, visually oriented theropod dinosaurs . Despite thyreophoran dinosaurs' possessing extensive dermal armor, some of the most extreme examples of anti-predator structures [8, 9], little direct evidence of predation on these and other dinosaur megaherbivores has been documented. Here we describe a new, exquisitely three-dimensionally preserved nodosaurid ankylosaur, Borealopelta markmitchelli gen. et sp. nov., from the Early Cretaceous of Alberta, which preserves integumentary structures as organic layers, including continuous fields of epidermal scales and intact horn sheaths capping the body armor. We identify melanin in the organic residues through mass spectroscopic analyses and observe lighter pigmentation of the large parascapular spines, consistent with display, and a pattern of countershading across the body. With an estimated body mass exceeding 1,300 kg, B. markmitchelli was much larger than modern terrestrial mammals that either are countershaded or experience significant predation pressure as adults. Presence of countershading suggests predation pressure strong enough to select for concealment in this megaherbivore despite possession of massive dorsal and lateral armor, illustrating a significant dichotomy between Mesozoic predator-prey dynamics and those of modern terrestrial systems.
The century-old idea that stripes make zebras cryptic to large carnivores has never been examined systematically. We evaluated this hypothesis by passing digital images of zebras through species-specific spatial and colour filters to simulate their appearance for the visual systems of zebras' primary predators and zebras themselves. We also measured stripe widths and luminance contrast to estimate the maximum distances from which lions, spotted hyaenas, and zebras can resolve stripes. We found that beyond ca. 50 m (daylight) and 30 m (twilight) zebra stripes are difficult for the estimated visual systems of large carnivores to resolve, but not humans. On moonless nights, stripes are difficult for all species to resolve beyond ca. 9 m. In open treeless habitats where zebras spend most time, zebras are as clearly identified by the lion visual system as are similar-sized ungulates, suggesting that stripes cannot confer crypsis by disrupting the zebra’s outline. Stripes confer a minor advantage over solid pelage in masking body shape in woodlands, but the effect is stronger for humans than for predators. Zebras appear to be less able than humans to resolve stripes although they are better than their chief predators. In conclusion, compared to the uniform pelage of other sympatric herbivores it appears highly unlikely that stripes are a form of anti-predator camouflage.
Although biologists routinely label animals as predators and prey, the ecological role of individuals is often far from clear. There are many examples of role reversals in predators and prey, where adult prey attack vulnerable young predators. This implies that juvenile prey that escape from predation and become adult can kill juvenile predators. We show that such an exposure of juvenile prey to adult predators results in behavioural changes later in life: after becoming adult, these prey killed juvenile predators at a faster rate than prey that had not been exposed. The attacks were specifically aimed at predators of the species to which they had been exposed. This suggests that prey recognize the species of predator to which they were exposed during their juvenile stage. Our results show that juvenile experience affects adult behaviour after a role reversal.
Camouflage, and in particular background-matching, is one of the most common anti-predator strategies observed in nature. Animals can improve their match to the colour/pattern of their surroundings through background selection, and/or by plastic colour 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 behind rapid colour change, but there is a considerable lack of information about slow colour change in the context of predation: the cues that initiate it, and the range of phenotypes that are produced. Here we show that peppered moth (Biston betularia) larvae respond to colour and luminance of the twigs they rest on, and exhibit a continuous reaction norm of phenotypes. When presented with a heterogeneous environment of mixed twig colours, individual larvae specialise crypsis towards one colour rather than developing an intermediate colour. Flexible colour change in this species has likely evolved in association with wind dispersal and polyphagy, which result in caterpillars settling and feeding in a diverse range of visual environments. This is the first example of visually induced slow colour change in Lepidoptera that has been objectively quantified and measured from the visual perspective of natural predators.
Tourism can be deleterious for wildlife because it triggers behavioral changes in individuals with cascading effects on populations and communities. Among these behavioral changes, animals around humans often reduce their fearfulness and antipredator responses towards humans. A straightforward prediction is that habituation to humans associated with tourism would negatively influence reaction to predators. This could happen indirectly, where human presence decreases the number of natural predators and thus prey become less wary, or directly, where human-habituated individuals become bolder and thus more vulnerable to predation. Building on ideas from the study of traits associated with domestication and urbanization, we develop a framework to understand how behavioral changes associated with nature-based tourism can impact individual fitness, and thus the demographic trajectory of a population.
Camouflage is perhaps the most widespread defence against predators in nature and an active area of interdisciplinary research. Recent work has aimed to understand what camouflage types exist (e.g. background matching, disruptive, and distractive patterns) and their effectiveness. However, work has almost exclusively focused on the efficacy of these strategies in preventing initial detection, despite the fact that predators often encounter the same prey phenotype repeatedly, affording them opportunities to learn to find those prey more effectively. The overall value of a camouflage strategy may, therefore, reflect both its ability to prevent detection by predators and resist predator learning. We conducted four experiments with humans searching for hidden targets of different camouflage types (disruptive, distractive, and background matching of various contrast levels) over a series of touch screen trials. As with previous work, disruptive coloration was the most successful method of concealment overall, especially with relatively high contrast patterns, whereas potentially distractive markings were either neutral or costly. However, high contrast patterns incurred faster decreases in detection times over trials compared to other stimuli. In addition, potentially distractive markings were sometimes learnt more slowly than background matching markings, despite being found more readily overall. Finally, learning effects were highly dependent upon the experimental paradigm, including the number of prey types seen and whether subjects encountered targets simultaneously or sequentially. Our results show that the survival advantage of camouflage strategies reflects both their ability to avoid initial detection (sensory mechanisms) and predator learning (perceptual mechanisms).
The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parent’s incubation bout varied from 1-19 h, whereas period length-the time in which a parent’s probability to incubate cycles once between its highest and lowest value-varied from 6-43 h. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or who actively protect their nest against predators. Rhythms entrainable to the 24-h light-dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.
Perceptual abilities of animals, like echolocating bats, are difficult to study because they challenge our understanding of non-visual senses. We used novel acoustic tomography to convert echoes into visual representations and compare these cues to traditional echo measurements. We provide a new hypothesis for the echo-acoustic basis of prey detection on surfaces. We propose that bats perceive a change in depth profile and an ‘acoustic shadow’ cast by prey. The shadow is more salient than prey echoes and particularly strong on smooth surfaces. This may explain why bats look for prey on flat surfaces like leaves using scanning behaviour. We propose that rather than forming search images for prey, whose characteristics are unpredictable, predators may look for disruptions to the resting surface (acoustic shadows). The fact that the acoustic shadow is much fainter on rougher resting surfaces provides the first empirical evidence for ‘acoustic camouflage’ as an anti-predator defence mechanism.
Invasive species cause catastrophic alterations to communities worldwide by changing the trophic balance within ecosystems. Ever since their introduction in the mid 1980’s common red lionfish, Pterois volitans, are having dramatic impacts on the Caribbean ecosystem by displacing native species and disrupting food webs. Introduced lionfish capture prey at extraordinary rates, altering the composition of benthic communities. Here we demonstrate that the extraordinary success of the introduced lionfish lies in its capacity to circumvent prey risk assessment abilities as it is virtually undetectable by prey species in its native range. While experienced prey damselfish, Chromis viridis, respond with typical antipredator behaviours when exposed to a common predatory rock cod (Cephalopholis microprion) they fail to visibly react to either the scent or visual presentation of the red lionfish, and responded only to the scent (not the visual cue) of a lionfish of a different genus, Dendrochirus zebra. Experienced prey also had much higher survival when exposed to the two non-invasive predators compared to P. volitans. The cryptic nature of the red lionfish has enabled it to be destructive as a predator and a highly successful invasive species.
- Proceedings. Biological sciences / The Royal Society
- Published almost 3 years ago
Ambush foragers use a hunting strategy that places them at risk of predation by both visual and olfaction-oriented predators. Resulting selective pressures have driven the evolution of impressive visual crypsis in many ambushing species, and may have led to the development of chemical crypsis. However, unlike for visual crypsis, few studies have attempted to demonstrate chemical crypsis. Field observations of puff adders (Bitis arietans) going undetected by several scent-orientated predator and prey species led us to investigate chemical crypsis in this ambushing species. We trained dogs (Canis familiaris) and meerkats (Suricata suricatta) to test whether a canid and a herpestid predator could detect B. arietans using olfaction. We also tested for chemical crypsis in five species of active foraging snakes, predicted to be easily detectable. Dogs and meerkats unambiguously indicated active foraging species, but failed to correctly indicate puff adder, confirming that B. arietans employs chemical crypsis. This is the first demonstration of chemical crypsis anti-predatory behaviour, though the phenomenon may be widespread among ambushers, especially those that experience high mortality rates owing to predation. Our study provides additional evidence for the existence of an ongoing chemically mediated arms race between predator and prey species.