Cryptic Prey Research Articles

The effect of distastefulness and conspicuous coloration on the post-attack rejection behaviour of predators and survival of prey

Aposematic insects use bright colours and/or distinct markings to advertise their toxins to potential predators. When toxins are bitter-tasting and detectable upon attack, birds are able to use taste when making decisions about whether or not to eat defended prey. Taste-rejection behaviour, when birds taste but do not ingest a prey item, is often assumed to increase the survival of defended prey, yet few empirical studies have investigated the post-attack survival rates of live defended insects. We used naive domestic chicks (Gallus gallus domesticus) foraging on live waxmoth larvae (Galleria mellonella) in a laboratory setting, where conspicuousness and distastefulness could be controlled and manipulated to investigate the effects of taste-rejection behaviour, as well as the associated handling behaviour, on post-attack survival of prey. We found that being distasteful increased the probability of being rejected by naive chicks, and taste-rejection behaviour tended to be more frequent when distasteful prey were conspicuous compared with when they were cryptic. Conspicuous coloration also appeared to affect predators’ assessment of prey distastefulness, with past experience strongly influencing the probability that conspicuous (but not cryptic) prey were rejected. However, in contrast to previous findings, there was no evidence that either distastefulness or conspicuousness altered how predators handled the prey before making a decision about whether or not to eat it, in any way that enhanced prey survival post-attack. Therefore, taste-rejection behaviour appears to be a useful measure of prey survival. Our results provide novel insights into the potential importance of signal conspicuousness for prey populations with variable defences, and highlight the need to consider the role of taste-rejection behaviour in mimicry dynamics.

Dimethylsulfoniopropionate (DMSP) Increases Survival of Larval Sablefish, Anoplopoma fimbria.

High concentrations of dimethylsulfoniopropionate (DMSP), a chemical compound released by lysed phytoplankton, may indicate high rates of grazing by zooplankton and may thus be a foraging cue for planktivorous fishes. Previous studies have shown that some planktivorous fishes and birds aggregate or alter locomotory behavior in response to this chemical cue, which is likely adaptive because it helps them locate prey. These behavioral responses have been demonstrated in juveniles and adults, but no studies have tested for effects on larval fish. Larvae suffer from high mortality rates and are vulnerable to starvation. While larvae are generally thought to be visual predators, they actually have poor vision and cryptic prey. Thus, larval fish should benefit from a chemical cue that provides information on prey abundance. We reared larval sablefish, Anoplopoma fimbria, for one week and supplemented feedings with varying concentrations of DMSP to test the hypothesis that DMSP affects larval survival. Ecologically relevant DMSP concentrations increased larval survival by up to 70 %, which has implications for production in aquaculture and recruitment in nature. These results provide a new tool for increasing larval production in aquaculture and also suggest that larvae may use DMSP as an olfactory cue. The release of DMSP may be a previously unappreciated mechanism through which phytoplankton affect larval survival and recruitment.

Distance-dependent switching of anti-predator behavior of frogs from immobility to fleeing

AbstractTo avoid predation, many animals are required to appropriately switch between immobility for crypsis and fleeing for escape. We conducted two staged-encounter experiments using a frog and a snake to examine factors that affect the occurrence of immobility and fleeing, and to evaluate the efficiency of them. The first experiment demonstrated that frogs initially exhibit immobility, when snakes are moving at a long distance, and then switch from immobility to fleeing at a shorter distance even when snakes have not detected them. The second experiment demonstrated that snakes at 400–800 mm distance detect only fleeing frogs, whereas snakes at 100 mm or closer detect both immobile and fleeing frogs. Thus, the ability of snakes to detect motionless frogs depends on the distance, and the distance-dependent switching can be considered an adaptive strategy of the frog. However, a previous model predicts that cryptic prey should flee immediately on seeing a predator or not flee until being detected by the predator. To explain this discordance, we propose two factors: engagement of intensive searching mode by predator at short distance and effects of sudden fleeing at close distance. We suggest incorporating them in future theory for better understanding of anti-predator strategy.

Sensitivity of a harbor seal (Phoca vitulina) to coherent visual motion in random dot displays.

Motion vision is one of the fundamental properties of the visual system and is involved in numerous tasks. Previous work has shown that harbor seals are able to perceive visual motion. Tying in with this experimental finding, we assessed the sensitivity of harbor seals to visual motion using random dot displays. In these random dot displays, either all or a percentage of the dots plotted in the display area move into one direction which is referred to as percent coherence. Using random dot displays allows determining motion sensitivity free from form or position cues. Moreover, when reducing the lifetime of the dots, the experimental subjects need to rely on the global motion over the display area instead of on local motion events, such as the streaks of single dots. For marine mammals, the interpretation of global motion stimuli seems important in the context of locomotion, orientation and foraging. The first experiment required the seal to detect coherent motion directed upwards in one out of two stimulus displays and psychophysical motion coherence detection thresholds were obtained ranging from 5% to 35% coherence. At the beginning of the second experiment, which was conducted to reduce the differential flickering of the motion stimulus as secondary cue, the seal was directly able to transfer from coherent motion detection to a discrimination of coherent motion direction, leftward versus rightward. The seal performed well even when the duration of the local motion event was extremely short in the last experiment, in which noise was programmed as random position noise. Its coherence threshold was determined at 23% coherence in this experiment. This motion sensitivity compares well to the performance of most species tested so far excluding monkeys, humans and cats. To conclude, harbor seals possess an effective global motion processing system. For seals, the interpretation of global and coherent motion might e. g. play a role in the interpretation of optic flow information or when breaking the camouflage of cryptic prey items.

Red fluorescence increases with depth in reef fishes, supporting a visual function, not UV protection.

Why do some marine fishes exhibit striking patterns of natural red fluorescence? In this study, we contrast two non-exclusive hypotheses: (i) that UV absorption by fluorescent pigments offers significant photoprotection in shallow water, where UV irradiance is strongest; and (ii) that red fluorescence enhances visual contrast at depths below −10 m, where most light in the ‘red’ 600–700 nm range has been absorbed. Whereas the photoprotection hypothesis predicts fluorescence to be stronger near the surface and weaker in deeper water, the visual contrast hypothesis predicts the opposite. We used fluorometry to measure red fluorescence brightness in vivo in individuals belonging to eight common small reef fish species with conspicuously red fluorescent eyes. Fluorescence was significantly brighter in specimens from the −20 m sites than in those from −5 m sites in six out of eight species. No difference was found in the remaining two. Our results support the visual contrast hypothesis. We discuss the possible roles fluorescence may play in fish visual ecology and highlight the possibility that fluorescent light emission from the eyes in particular may be used to detect cryptic prey.

Body size influences differently the detectabilities of colour morphs of cryptic prey

Body size and coloration may contribute to variation in performance and fitness among individuals, for instance by influencing vulnerability to predators. Yet, the combined effect of size and colou ...

Polar bear predatory behaviour reveals seascape distribution of ringed seal lairs

AbstractRinged seal (Pusa hispida) breeding distribution has been extensively studied across near‐shore habitats, but has received limited attention at a seascape scale due to the difficulty in accessing offshore sea ice environments. Employing highly visible predation attempts by polar bears (Ursus maritimus) on ringed seals in subnivean lairs observed by helicopter, the spatial relationship between predatory behaviour and ringed seal breeding habitat was examined. Resource selection functions were used to determine the relative probability of predation attempts on ringed seals in lairs as a function of habitat during a period of low ringed seal natality (2004–2006). Ringed seal pup kill locations were compared between years of low (2003–2006) and high (2007–2011) natality to assess the effect of reproductive output on habitat use. During years of low natality, polar bear hunting attempts were more likely in near‐shore fast ice, and pup kills were observed predominately in fast ice (fast = 65 %, pack = 29 %, P = 0.002) at a median distance of 36 km from shore. In years of high natality, pup kills were observed farther from shore (median = 46 km, P = 0.03), and there was no difference in the proportion of observations in fast ice and pack ice (fast = 43 %, pack = 52 %, P = 0.29). These results suggest that the facultative use of adjacent offshore pack ice by breeding ringed seals may be influenced by natality. This study illustrates how documenting the behaviour of a predator can facilitate insight into the distribution of a cryptic prey.

A direct comparison of the effectiveness of two anti‐predator strategies under field conditions

AbstractAposematism and crypsis are two widespread defensive strategies that have evolved in organisms to reduce attacks by predators. However, although both have been studied extensively, predation rates on unpalatable conspicuous prey have seldom been directly compared to those on palatable cryptic prey, and never in the field. In this study, we use established methods to compare the effectiveness of both defensive traits, by presenting artificial prey targets on trees where they were subject to attack by wild avian predators in a natural field setting. When partially consumed prey and those that had been completely removed were both treated as attacked by predators, there were no differences in attack rates between targets with the two defensive strategies. However, aposematic prey were completely consumed less often than cryptic prey, and partially consumed more often. This suggests that predators engage in taste rejection of unpalatable prey and/or feed on conspicuous prey more cautiously (‘go‐slow’ predation). We also observed significant differences in predation among experimental sites, in spite of their similarity and relatively close proximity, and among trials, which suggests that prey may experience highly variable predation in the wild. If aposematic prey are capable of surviving attacks by predators, then this represents a potential defensive benefit of aposematism over crypsis.

Revealed by conspicuousness: distractive markings reduce camouflage

Animal camouflage is a textbook example of natural selection. Despite substantial progress, one historical theory remains controversial: that conspicuous “distractive” markings draw predator attention away from the prey outline, preventing detection. Here, we present evidence from 4 experiments to resolve this controversy. In field experiments, we measured bird predation on artificial cryptic prey that were either unmarked or had distractive markings of various attributes (number, color, and location). Prey with 3 high-contrast distractive markings, and with markings located away from the body outline, suffered reduced survival compared with unmarked controls or prey with low-contrast markings. There was no effect of small single markings with different colors on the survival of targets. In 2 computer-based experiments with human subjects searching for hidden targets, distractive markings of various types (number, size, and location) reduced detection times compared with controls. This effect was greatest for targets that had large or 3 markings. In addition, small and centrally placed markings facilitated faster learning. Therefore, these 2 experimental approaches show that distractive markings are detrimental to camouflage, both facilitating initial detection and increasing the speed of predator learning. Our experiments also suggest that learning of camouflaged prey is dependent on the type of camouflage present. Contrary to current and historical discussion, conspicuous markings are more likely to impair camouflage than enhance it, presenting important implications for the optimization of prey coloration in general. Key wor ds: camouflage, conspicuousness, distraction, learning, predation, vision. [Behav Ecol]

Aposematism and the Handicap Principle

Aposematic prey use conspicuous warning signals to advertise their defenses to predators. It has long been recognized that the efficiency of a warning signal may be reduced if poorly defended prey (automimics) are present in the population. The handicap principle suggests that the use of warning signals by poorly defended prey may be kept in check if signaling is costly. Three mechanisms that involve signal costs have been proposed to facilitate honest warning signals in prey: go-slow behavior in predators, resource allocation trade-offs, and costs of detection alone. We study all three in a unified game-theoretical framework. We find that the go-slow mechanism and the resource allocation mechanism can introduce differential benefits and differential costs of signaling, respectively, and can support honest signaling in accordance with the handicap principle. When honest signaling is maintained by the go-slow mechanism, conspicuous prey will necessarily suffer more attacks on average than cryptic prey. In contrast, when honest signaling is maintained by the resource allocation mechanism, cryptic prey will suffer more attacks. The detection cost mechanism lacks differential costs and benefits, and its potential for maintaining honest signaling equilibria is limited. We relate our results to intra- and interspecific correlations between conspicuousness and defense.

Protection by association: evidence for aposematic commensalism

Aposematism is a well known and widely used strategy for reducing predation by conspicuous signalling of unprofitability. However, the increased conspicuousness could make this strategy costly if there are no secondary defences to back the signal up. This has made the elucidation of the evolutionary mechanisms for aposematism and that of the closely-related Batesian and Mullerian mimicry difficult. The present study aims to test whether cryptic and nondefended prey could reduce their predation risk by grouping with aposematic and defended prey. To do this, we used groups of artificial baits that were either cryptic and palatable or conspicuous and unpalatable, along with the corresponding control treatments. These were then presented in mixed and homogeneous treatment groups within a field setting and the local wild bird assemblage was allowed to select and remove baits at will. The results obtained show that undefended non-aposematic prey can benefit by grouping with aposematic prey, with no evidence that predation rates for aposematic prey were adversely affected by this association. These results provide insights into the evolution of Batesian mimicry.

Colour-independent shape recognition of cryptic predators by bumblebees

Predators hunting for cryptic prey use search images, but how do prey search for cryptic predators? We address this question using the interaction between bumblebees and the colour-changing crab spider Misumena vatia which can camouflage itself on some flowers. In laboratory experiments, we exposed bumblebees to an array of flowers concealing robotic predators (a trapping mechanism combined with a 3D life-sized model of a crab spider or a circle). Groups of bees were trained to avoid either cryptic yellow spiders or yellow circles (equal area to the spiders) or remained predator naive. The bees were then exposed to a new patch of white flowers containing some cryptic predators (either white spiders, white circles or a mixture of both). We monitored individual foraging choices and used a 3D video tracking system to quantify the bees’ flight behaviour. The bees trained to avoid cryptic spiders, chose 40% fewer spider-harbouring flowers than expected by chance, but were indifferent to cryptic circles. They also aborted a higher proportion of landings on flowers harbouring spiders, ultimately feeding from half as many ‘dangerous’ flowers as naive bees. Previous encounters with cryptic spiders also influenced the flight behaviour of bees in the new flower patch. Experienced bees spent more time inspecting the flowers they chose to reject (both with and without concealed spiders) and scanned from side to side more in front of the flowers to facilitate predator detection. We conclude that bees disentangle shape from colour cues and thus can form a generalised search image for spider shapes, independent of colour.

Prey pattern regularity and background complexity affect detectability of background-matching prey

We investigated how regularity of prey color pattern affects crypsis and how visual complexity of the background affects prey detection. We performed 2 predation experiments with artificial prey and backgrounds, using blue tits (Cyanistes caeruleus )a s predators. In experiment 1, we found that contrary to a previous hypothesis, a pattern with repeated background-matching pattern element shapes was not easier to detect than a pattern with variable background-matching shapes. Increased background complexity with respect to shape diversity and complexity made prey detection more difficult. In experiment 2, we tested how spatial regularity of background-matching pattern elements affects crypsis. We found that spatially irregular prey with randomly placed pattern elements were harder to detect on both simple and complex backgrounds compared with spatially regular prey that had the elements aligned. Increased background element shape complexity made both prey categories harder to detect. In conclusion, our study shows that spatial regularity of prey pattern but not regularity due to invariable pattern element shapes deteriorates crypsis. Visually complex backgrounds and specifically those consisting of elements with complex shapes make detection of cryptic prey difficult. Key words: background matching, camouflage, crypsis, predation, prey coloration, spatial regularity. [Behav Ecol]

Learning and context-specific exploration behaviour in hatchery and wild brown trout

In this study we investigate whether rearing environment (wild vs. hatchery) affects the ability of brown trout parr ( Salmo trutta) to learn two foraging tasks. Hatchery- and wild-reared brown trout were trained in two different foraging tasks: locating food hidden in a maze and finding a cryptic prey, and their performance within and across tasks was compared. Fish reduced their search time for cryptic prey, but not maze search time, by learning. In contrast to most previous studies hatchery-reared trout generally tended to be more successful feeders and showed faster learning than wild trout when foraging on cryptic prey. This appeared to be due to motivational effects rather than based on cognitive skills. In addition, we examine whether exploration behaviour in brown trout is repeatable across time and context (i.e. reflecting a behavioural syndrome). Individual exploration tendency was repeatable within tasks, suggesting the occurrence of personality in brown trout. However, individuals that were fast explorers in the cryptic prey task were not necessarily fast to explore the maze. Thus, a context-specific behavioural syndrome was found to best explain exploratory behaviour for both hatchery and wild trout. However, repeatability of exploration behaviour within tasks differed between hatchery and wild trout, where wild trout were found to be more consistent in their exploration strategy.

Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues

1. Olfactory predator search processes differ fundamentally to those based on vision, particularly when odour cues are deposited rather than airborne or emanating from a point source. When searching for visually cryptic prey that may have moved some distance from a deposited odour cue, cue context and spatial variability are the most likely sources of information about prey location available to an olfactory predator. 2. We tested whether the house mouse (Mus domesticus), a model olfactory predator, would use cue context and spatial variability when searching for buried food items; specifically, we tested the effect of varying cue patchiness, odour strength, and cue-prey association on mouse foraging success. 3. Within mouse- and predator-proof enclosures, we created grids of 100 sand-filled Petri dishes and buried peanut pieces in a set number of these patches to represent visually cryptic 'prey'. By adding peanut oil to selected dishes, we varied the spatial distribution of prey odour relative to the distribution of prey patches in each grid, to reflect different levels of cue patchiness (Experiment 1), odour strength (Experiment 2) and cue-prey association (Experiment 3). We measured the overnight foraging success of individual mice (percentage of searched patches containing prey), as well as their foraging activity (percentage of patches searched), and prey survival (percentage of unsearched prey patches). 4. Mouse foraging success was highest where odour cues were patchy rather than uniform (Experiment 1), and where cues were tightly associated with prey location, rather than randomly or uniformly distributed (Experiment 3). However, when cues at prey patches were ten times stronger than a uniformly distributed weak background odour, mice did not improve their foraging success over that experienced when cues were of uniform strength and distribution (Experiment 2). 5. These results suggest that spatial variability and cue context are important means by which olfactory predators can use deposited odour cues to locate visually cryptic prey. They also indicate that chemical crypsis can disrupt these search processes as effectively as background matching in visually based predator-prey systems.

Disengtangling the evolution of weak warning signals: high detection risk and low production costs of chemical defences in gregarious pine sawfly larvae

Evolution of costly secondary defences for a cryptic prey is puzzling, if the prey is already well protected by camouflage. However, if the chemical defence is not sufficient to deter all predators, selection can favour low signal intensity in defended prey. Alternatively, if the costs of chemical defence are low or cost-free, chemical defences can be expected to evolve also for non-signalling prey, particularly if conspicuous signalling is costly. We tested these assumptions with pine sawfly larvae (Neodiprion sertifer and Diprion pini) that are cryptically coloured and chemically defended with resin acids sequestered from their host plant (Pinus sp.). Larvae feed in large aggregations, which we hypothesise could function as a signal of unprofitability. Our results show that even though the birds found N. sertifer larvae unprofitable in the controlled laboratory assays, they continued attacking and consuming them in the wild. When we tested the signal value of aggregation we found that a large group size did not offer protection for a defended larva: the survival was higher in groups of 10 individuals compared to groups of 50, suggesting increased detectability costs for individuals in larger groups. Finally, we tested how costly the production and maintenance of a chemical defence is for D. pini larvae by manipulating the resin acid content of the diet. We did not find any life history or immunological costs of the chemical defence for the larvae. In contrast, pupal weights were higher on the high resin diet than on the low resin diet. Also, larvae were able to produce higher amounts of defence fluids on the high diet than on the low diet. Thus, our result suggests high detectability costs and low production costs of defences could explain why some unprofitable species have not evolved conspicuous signals.

Can the dietary conservatism of predators compensate for positive frequency dependent selection against rare, conspicuous prey?

The evolution of conspicuous colouration in prey is puzzling because such coloration attracts the attention of predators. Anti-apostatic selection, in which rare prey forms are predated disproportionately often, is a second potential obstacle to the evolution of conspicuous colouration in prey, as bright novel prey forms are likely to be very rare when they first appear in populations. It has recently been postulated that dietary conservatism in predators, an extended feeding avoidance of novel prey, would allow novel conspicuous prey to survive and multiply despite anti-apostatic and conspicuousness effects. We tested this hypothesis for a novel prey type arising in an otherwise cryptic population, providing a direct test of whether anti-apostatic selection or the predators’ wariness to attack the novel prey type is the more important force acting on the novel conspicuous prey. We conducted our experiment in the “Novel World”; an experimental system designed to test predators’ foraging decisions in a large landscape. We found that the conspicuous, novel prey suffered high initial costs of conspicuousness compared with cryptic prey, since most of these prey were attacked during the first “generation”, with no opportunity to “reproduce”. However, a subset of the 17 birds (24%) were following a dietary conservative foraging strategy and they were reluctant to eat the novel prey. Interestingly these birds were not more neophobic or less explorative. Our data demonstrate how difficult it is for the novel conspicuous prey to survive in cryptic populations, but they also highlight the importance of the predator’s foraging strategies in helping to promote the evolution and maintenance of aposematism.

Crypsis influences escape decisions in the Round-tailed Horned Lizard (Phrynosoma modestum)

Flight initiation distance (predator–prey distance when escape begins) increases as predation risk increases. Prey should have longer flight initiation distance when their background, movement, or current posture reduces crypsis. Flight initiation distance of ectotherms may increase at lower body temperature to compensate for slower running speed. However, for cryptic prey, fleeing might increase the probability of being detected. The Round-tailed Horned Lizard ( Phrynosoma modestum Girard, 1852) is eucryptic and resembles small stones. We predicted that flight initiation distance by P. modestum is shorter among stones than on uniform sand. Because movement and upright posture disrupt crypsis, we predicted that flight initiation distance is greater after movement and when standing than when still and lying on the ground. As predicted, flight initiation distances were shorter on a rocky than sandy area, when lying flat than standing, and while immobile than after moving. We measured running speed and flight initiation distance to determine relationships among body temperature, speed, and escape decisions. Running speed and flight initiation distance were reduced at lower body temperature, suggesting that crypsis reinforced by immobility is more advantageous than longer flight initiation distance for cool, slow lizards. The lizards adjusted escape decisions to current effectiveness of crypsis and escape ability.

Cryptic interference competition in swans foraging on cryptic prey

Interference can be defined as the reduction of intake rate caused by the presence of congeneric individuals. However, surrounding congeneric individuals may also accelerate food depletion. Therefore, it is difficult to quantify interference (contest) and exploitative (scramble) competition separately, particularly in the field. In an individual-based model, where food was immediately replenished in patches after a foraging bout, we isolated the effect of interference competition. In this way, we investigated how interference shapes the intake rates of flocking Bewick’s swans, Cygnus bewickii, consuming tubers of fennel pondweed, Potamogeton pectinatus. The model predicted that intake rate declines with increasing swan density, and that the rate of decline is greater in subordinate birds than in dominant birds. Subordinate birds suffered a large reduction in intake rate at high densities because they spent a large proportion of the time avoiding more dominant individuals. A major decline in intake rate of subordinates occurred close to the maximum swan densities observed in the field. We expected subordinates to leave high-density flocks and look for another foraging location: interference competition seemed to regulate the maximum swan flock density in the field. Hence, the mean population intake rate at realized densities was only slightly lower than in the absence of interference. As interference occurred mainly as avoidance behaviour, which is difficult to observe in the field, it might commonly remain cryptic for the observer. Our results may explain other field studies where interference competition seemed to be of lesser importance.

Plesiomorphic Escape Decisions in Cryptic Horned Lizards (Phrynosoma) Having Highly Derived Antipredatory Defenses

AbstractEscape theory predicts that the probability of fleeing and flight initiation distance (predator–prey distance when escape begins) increase as predation risk increases and decrease as escape cost increases. These factors may apply even to highly cryptic species that sometimes must flee. Horned lizards (Phrynosoma) rely on crypsis because of coloration, flattened body form, and lateral fringe scales that reduce detectability. At close range they sometimes squirt blood‐containing noxious substances and defend themselves with cranial spines. These antipredatory traits are highly derived, but little is known about the escape behavior of horned lizards. Of particular interest is whether their escape decisions bear the same relationships to predation risk and opportunity costs of escaping as in typical prey lacking such derived defenses. We investigated the effects of repeated attack and direction of predator turning on P. cornutum and of opportunity cost of fleeing during a social encounter in P. modestum. Flight initiation distance was greater for the second of two successive approaches and probability of fleeing decreased as distance between the turning predator and prey increased, but was greater when the predator turned toward than away from a lizard. Flight initiation distance was shorter during social encounters than when lizards were solitary. For all variables studied, risk assessment by horned lizards conforms to the predictions of escape theory and is similar to that in other prey despite their specialized defenses. Our findings show that these specialized, derived defenses coexist with a taxonomically widespread, plesiomorphic method of making escape decisions. They suggest that escape theory based on costs and benefits, as intended, applies very generally, even to highly cryptic prey that have specialized defense mechanisms.