Predator Confusion Research Articles

Schooling Fish from a New, Multimodal Sensory Perspective.

The acoustic hypothesis suggests that schooling can result in several benefits. (1) The acoustic pattern (AP) (pressure waves and other water movements) produced by swimming are likely to serve as signals within fish shoals, communicating useful spatial and temporal information between school members, enabling synchronized locomotion and influencing join, stay or leave decisions and shoal assortment. (2) Schooling is likely to reduce the masking of environmental signals, e.g., by auditory grouping, and fish may achieve windows of silence by simultaneously stopping their movements. (3) A solitary swimming fish produces an uncomplicated AP that will give a nearby predator's lateral line organ (LLO) excellent information, but, if extra fish join, they will produce increasingly complex and indecipherable APs. (4) Fishes swimming close to one another will also blur the electrosensory system (ESS) of predators. Since predators use multimodal information, and since information from the LLO and the ESS is more important than vision in many situations, schooling fish may acquire increased survival by confusing these sensory systems. The combined effects of such predator confusion and other acoustical benefits may contribute to why schooling became an adaptive success. A model encompassing the complex effects of synchronized group locomotion on LLO and ESS perception might increase the understanding of schooling behavior.

Microplastics in the Deep: Comparing Dietary and Plastic Ingestion Data between Two Mediterranean Bathyal Opportunistic Feeder Species, Galeus melastomus, Rafinesque, 1810 and Coelorinchus caelorhincus (Risso, 1810), through Stomach Content Analysis

Marine plastic pollution is currently an issue of mounting concern around the world. Stomach content of marine fish has been increasingly used as a valid proxy for detecting the presence of such a pollutant in marine biota, both for coastal and deep-water environments. Although ingestion of microplastics has been reported in an increasing number of species, the patterns of ingestion still remain unclear, depending closely on the interaction between the species and types of microplastics involved. In this context, we analysed and compared the stomach contents of two bathyal dwelling opportunistic feeder species namely Galeus melastomus and Coelorinchus caelorhincus. In particular, we analysed microplastic items according to their dimension, morphology and colour, and diet’s variation with size obtained through prey identification. Both species showed a higher frequency of occurrence of the blue filament-like middle-sized microplastics (1.01–4.75 mm) compared with the other categories, although this pattern was much more marked in C. caelorhincus than in G. melastomus. The latter conversely showed a larger array of ingested plastic items in terms of shape and colour. Matching plastic ingestion with dietary data suggested potential predator confusion occurring in C. caelorhincus through active mis-selection of a defined type of microplastic instead of some particular family of polychaetes, which resemble in shape, size, and color to that type. Otherwise, G. melastomus appeared more prone to a random ingestion of a larger array of microplastic items because of a more generalistic and less selective feeding strategy. Although further validation is needed, stomach contents of the two species showed evidence strong enough to be considered as potential bioindicator species of microplastic pollution, as required by the Marine Strategy Framework Directive for monitoring this pollutant in the marine environment.

Collective Predator Perception Advertisement in Fish

The idea that prey might advertise their perception of predators to avoid attacks has received considerable attention in the literature. However, evidence for reduced attack frequencies or attack success in predators as a result of perception advertisement in prey is limited or indirect. Here we present a field study which investigated the benefits of waves produced by fish at the water surface when diving down collectively in response to attacks of avian predators. Instead of merely escaping, fish engaged in surface waves that were highly conspicuous, repetitive and rhythmic involving many thousands of individuals for up to 2 min. Experimentally-induced fish waves doubled the time birds waited until their next attack therefore substantially reducing attack frequency. In one avian predator, capture probability, too, decreased with wave number and birds switched perches in response to wave displays more often than in control treatments suggesting that they directed their attacks elsewhere. Taken together these results support fish waves’ function of perception advertisement. A predator confusion effect is also possible but so far is not known to be associated with waving behaviour especially given that rhythmic waving could make prey more predictable. Collectively produced perception advertisements raise some intriguing questions of how fish synchronise to produce such signals and which pathway has led to their evolution.

Odd one in: Oddity within mixed‐species shoals does not affect shoal preference by vagrant tropical damselfish in the presence or absence of a predator

AbstractGrouping behaviour displayed by animals is usually attributed to predation and foraging‐related benefits. The mechanisms of predator protection and foraging efficiency are diverse and often produce conflicting drivers of grouping behaviour. One key conflict is that between group size and phenotypic oddity. Theoretically, individuals should choose the largest available group due to multiple mechanisms associated with “safety in numbers”. However, individuals should also choose the most phenotypically similar group members due to the “predator confusion effect”. This conflict is particularly important within the context of mixed‐species groups because, while their formation may facilitate large group size, phenotypic differences between species may be costly due to oddity. To investigate the interacting effects of shoal size, composition and predator presence on grouping decisions, choice experiments were conducted using displaced tropical damselfish, Abudefduf vaigiensis, settling in temperate south‐eastern Australia (termed vagrants) as a model species. Contrary to predictions, A. vaigiensis displayed no preference for single‐ over mixed‐species shoals, with or without a predator present. These results suggest that shoal composition may not be an important driver of shoal choice in this system. Further, A. vaigiensis showed no preference for larger mixed‐species shoals over smaller single‐species shoals. These outcomes are discussed within the context of climate change‐driven redistribution of A. vaigiensis in temperate south‐eastern Australia.

Predator Eavesdropping in a Mixed-Species Environment: How Prey Species May Use Grouping, Confusion, and the Cocktail Party Effect to Reduce Predator Detection

The field of predator eavesdropping concentrates on the detection by a predator or parasite of signals that prey direct at conspecifics, and the subsequent evolution by prey to avoid or lessen such detection. Here, we first point out that signaling prey species are often found in mixed-species moving groups or stationary aggregations, and ask the question of how simultaneous signaling, by members of one species or more, might affect predator eavesdropping behavior and the composition of the groups themselves. The detection risk of prey species will be affected by the other species they associate with, and prey should generally avoid joining a group with more detectable species. Yet prey may select to join other species that are preferred by predators, diluting their own risk of attack, as long as that does not lead to substantially greater detection and thereby increased predation. We next review the evidence that prey grouping and collective responses when attacked can confuse predators, leading to lower capture rates. Evidence for this confusion effect mostly involves visually orienting predators. We then ask if a similar phenomenon could occur when animals in a group simultaneously send acoustic signals, and find relevant evidence for predator confusion under such situations in the literature associated with the “cocktail party effect”. As confusion is heightened by similarities among mixed-species group members, this provides a force at ecological or evolutionary timescales to make species that associate in groups, and their signals, more similar to each other. However, heterogeneous mixed-species groups may be favored if species are differentially preferred as prey. We suggest experiments to examine whether the success rates of acoustically orienting predators depend on the group size of their mixed-species prey. More observations on the relative positions of conspecifics and heterospecifics in space, and the temporal association of their signals, will also increase our understanding of the relationship between mixed-species grouping and predator eavesdropping.

Phenotypic assortment by body shape in wild-caught fish shoals

Phenotypic variation plays a critical role in determining the structural organisation and ecological function of wild populations. Animal groups are often structured according to factors such as species, sex, body size and parasite load, but it is unclear whether body shape also influences patterns of social organisation, and thus contributes to population phenotypic structure. Here, we use geometric morphometric analyses to determine whether wild-caught shoals of a freshwater fish, the western rainbowfish (Melanotaenia australis), are structured according to body size and shape. Using randomisation analyses, we show that the level of variation in size and shape observed in natural group assemblages is lower than that expected under a null model of random shoal composition. In addition, we found evidence of further phenotypic structuring along an upstream-downstream environmental gradient. The putative benefits of morphological assortment include a reduction in predation risk (due to prey oddity and predator confusion effects) and increased hydrodynamic or foraging efficiency. We suggest that morphological variation is a neglected component of population social organisation that can affect population processes, such as patterns of gene flow, and ecological interactions, such as predator-prey dynamics.

Further Comments on Ear-flashing as a Predator Confusion Adaptation in Hares (Lepus)

Further Comments on Ear-flashing as a Predator Confusion Adaptation in Hares (<i>Lepus</i>)

Observations of female and mixed sex swarming behaviour in Culicoides Latreille, 1809 (Diptera: Ceratopogonidae)

Abstract Female swarming behaviour has rarely been described in Culicoides. Previous records of female swarms have only been described for females swarming in mixed swarms together with males. Two new observations of Culicoides swarms in Sweden are described here: a mixed swarm with females of Culicoides obsoletus / gornostaevae and males of C. gornostaevae, and a purely female swarm of C. impunctatus. Swarming behaviour can facilitate predator confusion. Swarming behaviour is therefore an evolutionary advantage that can explain mixed species swarms and purely female swarms.

Birds of a feather flock together: Insights into starling murmuration behaviour revealed using citizen science.

Pre-roost murmuration displays by European starlings Sturnus vulgaris are a spectacular example of collective animal behaviour. To date, empirical research has focussed largely on flock movement and biomechanics whereas research on possible causal mechanisms that affect flock size and murmuration duration has been limited and restricted to a small number of sites. Possible explanations for this behaviour include reducing predation through the dilution, detection or predator confusion effects (the “safer together” hypotheses) or recruiting more birds to create larger (warmer) roosts (the “warmer together” hypothesis). We collected data on size, duration, habitat, temperature and predators from >3,000 murmurations using citizen science. Sightings were submitted from 23 countries but UK records predominated. Murmurations occurred across a range of habitats but there was no association between habitat and size/duration. Size increased significantly from October to early February, followed by a decrease until the end of the season in March (overall mean 30,082 birds; maximum 750,000 birds). Mean duration was 26 minutes (± 44 seconds SEM). Displays were longest at the start/end of the season, probably due to a significant positive relationship with day length. Birds of prey were recorded at 29.6% of murmurations. The presence of predators including harrier Circus, peregrine Falco peregrinus, and sparrowhawk Accipiter nisus was positively correlated with murmuration size (R2 = 0.401) and duration (R2 = 0.258), especially when these species were flying near to, or actively engaging with, starlings. Temperature was negatively correlated with duration but the effect was much weaker than that of day length. When predators were present, murmurations were statistically more likely to end with all birds going down en masse to roost rather than dispersing from the site. Our findings suggest that starling murmurations are primarily an anti-predator adaptation rather than being undertaken to attract larger numbers of individuals to increase roost warmth.

A Sensory-Driven Trade-Off between Coordinated Motion in Social Prey and a Predator's Visual Confusion.

Social animals are capable of enhancing their awareness by paying attention to their neighbors, and prey found in groups can also confuse their predators. Both sides of these sensory benefits have long been appreciated, yet less is known of how the perception of events from the perspectives of both prey and predator can interact to influence their encounters. Here we examined how a visual sensory mechanism impacts the collective motion of prey and, subsequently, how their resulting movements influenced predator confusion and capture ability. We presented virtual prey to human players in a targeting game and measured the speed and accuracy with which participants caught designated prey. As prey paid more attention to neighbor movements their collective coordination increased, yet increases in prey coordination were positively associated with increases in the speed and accuracy of attacks. However, while attack speed was unaffected by the initial state of the prey, accuracy dropped significantly if the prey were already organized at the start of the attack, rather than in the process of self-organizing. By repeating attack scenarios and masking the targeted prey’s neighbors we were able to visually isolate them and conclusively demonstrate how visual confusion impacted capture ability. Delays in capture caused by decreased coordination amongst the prey depended upon the collection motion of neighboring prey, while it was primarily the motion of the targets themselves that determined capture accuracy. Interestingly, while a complete loss of coordination in the prey (e.g., a flash expansion) caused the greatest delay in capture, such behavior had little effect on capture accuracy. Lastly, while increases in collective coordination in prey enhanced personal risk, traveling in coordinated groups was still better than appearing alone. These findings demonstrate a trade-off between the sensory mechanisms that can enhance the collective properties that emerge in social animals and the individual group member’s predation risk during an attack.

Antipredator Vocalization Usage in the Male Ring-Tailed Lemur (Lemur catta)

The ring-tailed lemur (Lemur catta) is a group-living strepsirrhine primate endemic to Madagascar that faces considerable predation pressure from aerial and terrestrial predators. This species engages in mobbing and vigilance behavior in response to predators, and has referential alarm vocalizations. Because L. catta is female dominant, less is known about the alarm calls of males. We tested 3 hypotheses for male antipredator vocalization behavior on L. catta at the Bezà Mahafaly Special Reserve in Madagascar: the predator confusion, group maintenance, and predation risk allocation hypotheses. We found support for 2 hypotheses. When a male L. catta made an antipredator call, other group members vocalized in response. Dominant males did not make alarm calls at higher rates than subordinate males. Predators were more abundant on the western side of Parcel 1, but an even greater number of antipredator vocalizations occurred in this area than predator abundance warranted. We show that male L. catta consistently participated in group-level antipredator vocalization usage in high-risk locations. Although female L. catta are known to hold the primary role in group defense, male L. catta are also key participants in group-wide behaviors that may confuse or drive away predators.

Batesian mimics influence the evolution of conspicuousness in an aposematic salamander.

Conspicuousness, or having high contrast relative to the surrounding background, is a common feature of unpalatable species. Several hypotheses have been proposed to explain the occurrence of conspicuousness, and while most involve the role of conspicuousness as a direct signal of unpalatability to potential predators, one hypothesis suggests that exaggerated conspicuousness may evolve in unpalatable species to reduce predator confusion with palatable species (potential Batesian mimics). This hypothesis of antagonistic coevolution between palatable and unpalatable species hinges on the 'cost of conspicuousness', in which conspicuousness increases the likelihood of predation more in palatable species than in unpalatable species. Under this mimicry scenario, four patterns are expected: (i) mimics will more closely resemble local models than models from other localities, (ii) there will be a positive relationship between mimic and model conspicuousness, (iii) models will be more conspicuous in the presence of mimics, and (iv) when models and mimics differ in conspicuousness, mimics will be less conspicuous than models. We tested these predictions in the salamander mimicry system involving Notophthalmus viridescens (model) and one colour morph of Plethodon cinereus (mimic). All predictions were supported, indicating that selection for Batesian mimicry not only influences the evolution of mimics, but also the evolution of the models they resemble. These findings indicate that mimicry plays a large role in the evolution of model warning signals, particularly influencing the evolution of conspicuousness.

Simulating predator attacks on schools: Evolving composite tactics

One hypothesis about the origins and evolution of coordinated animal movements is that they may serve as a defensive mechanism against predation. Earlier studies of the possible evolution of coordinated movement in prey concentrated on predators with simple attack tactics. Numerous studies, however, suggest that to overcome the apparent defensive mechanisms which grouping and coordinated movement may provide to prey, predators in nature appear to use elaborate target selection and pursuit/hunting tactics. We here study predators that use composite tactics, (a) predators that in successive attacks based on probability choose one of several simple attack tactics, (b) predators that first disperse prey and then pick off isolated individuals. We develop an individual based model of a group of prey that is attacked by a solitary predator agent. By using genetic algorithms, we enable the predator agent to adapt (a) the probability that a specific tactic will be selected in the next attack, (b) the distance at which it stops dispersing the prey and the radius within which it searches for the most isolated prey. With a direct competition of the evolved predator agents we examine which is the better tactic against a group of prey moving in a polarized cohesive manner in three different settings. Our results suggest that, (a) a delayed response is an efficient advanced prey defence tactic, (b) predator confusion plays an important role in the evolution of composite tactics, and (c) when confusion is at play, the dispersing predator is a much better hunter, capable of at least partially diminishing the effectiveness of the prey's delayed response.

Predator confusion is sufficient to evolve swarming behaviour

Swarming behaviours in animals have been extensively studied owing to their implications for the evolution of cooperation, social cognition and predator-prey dynamics. An important goal of these studies is discerning which evolutionary pressures favour the formation of swarms. One hypothesis is that swarms arise because the presence of multiple moving prey in swarms causes confusion for attacking predators, but it remains unclear how important this selective force is. Using an evolutionary model of a predator-prey system, we show that predator confusion provides a sufficient selection pressure to evolve swarming behaviour in prey. Furthermore, we demonstrate that the evolutionary effect of predator confusion on prey could in turn exert pressure on the structure of the predator's visual field, favouring the frontally oriented, high-resolution visual systems commonly observed in predators that feed on swarming animals. Finally, we provide evidence that when prey evolve swarming in response to predator confusion, there is a change in the shape of the functional response curve describing the predator's consumption rate as prey density increases. Thus, we show that a relatively simple perceptual constraint--predator confusion--could have pervasive evolutionary effects on prey behaviour, predator sensory mechanisms and the ecological interactions between predators and prey.

Why do fish school?

Abstract Synchronized movements (schooling) emit complex and overlapping sound and pressure curves that might confuse the inner ear and lateral line organ (LLO) of a predator. Moreover, prey-fish moving close to each other may blur the electro-sensory perception of predators. The aim of this review is to explore mechanisms associated with synchronous swimming that may have contributed to increased adaptation and as a consequence may have influenced the evolution of schooling. The evolutionary development of the inner ear and the LLO increased the capacity to detect potential prey, possibly leading to an increased potential for cannibalism in the shoal, but also helped small fish to avoid joining larger fish, resulting in size homogeneity and, accordingly, an increased capacity for moving in synchrony. Water-movements and incidental sound produced as by-product of locomotion (ISOL) may provide fish with potentially useful information during swimming, such as neighbour body-size, speed, and location. When many fish move close to one another ISOL will be energetic and complex. Quiet intervals will be few. Fish moving in synchrony will have the capacity to discontinue movements simultaneously, providing relatively quiet intervals to allow the reception of potentially critical environmental signals. Besides, synchronized movements may facilitate auditory grouping of ISOL. Turning preference bias, well-functioning sense organs, good health, and skillful motor performance might be important to achieving an appropriate distance to school neighbors and aid the individual fish in reducing time spent in the comparatively less safe school periphery. Turning preferences in ancestral fish shoals might have helped fish to maintain groups and stay in formation, reinforcing aforementioned predator confusion mechanisms, which possibly played a role in the lateralization of the vertebrate brain.

UV Photoreceptors and UV-Yellow Wing Pigments inHeliconiusButterflies Allow a Color Signal to Serve both Mimicry and Intraspecific Communication

Mimetic wing coloration evolves in butterflies in the context of predator confusion. Unless butterfly eyes have adaptations for discriminating mimetic color variation, mimicry also carries a risk of confusion for the butterflies themselves. Heliconius butterfly eyes, which express recently duplicated ultraviolet (UV) opsins, have such an adaptation. To examine bird and butterfly color vision as sources of selection on butterfly coloration, we studied yellow wing pigmentation in the tribe Heliconiini. We confirmed, using reflectance and mass spectrometry, that only Heliconius use 3-hydroxy-DL-kynurenine (3-OHK), which looks yellow to humans but reflects both UV- and long-wavelength light, whereas butterflies in related genera have chemically unknown yellow pigments mostly lacking UV reflectance. Modeling of these color signals reveals that the two UV photoreceptors of Heliconius are better suited to separating 3-OHK from non-3-OHK spectra compared with the photoreceptors of related genera or birds. The co-occurrence of potentially enhanced UV vision and a UV-reflecting yellow wing pigment could allow unpalatable Heliconius private intraspecific communication in the presence of mimics. Our results are the best available evidence for the correlated evolution of a color signal and color vision. They also suggest that predator visual systems are error prone in the context of mimicry.

Balancing the dilution and oddity effects: decisions depend on body size.

BackgroundGrouping behaviour, common across the animal kingdom, is known to reduce an individual's risk of predation; particularly through dilution of individual risk and predator confusion (predator inability to single out an individual for attack). Theory predicts greater risk of predation to individuals more conspicuous to predators by difference in appearance from the group (the ‘oddity’ effect). Thus, animals should choose group mates close in appearance to themselves (eg. similar size), whilst also choosing a large group.Methodology and Principal FindingsWe used the Trinidadian guppy (Poecilia reticulata), a well known model species of group-living freshwater fish, in a series of binary choice trials investigating the outcome of conflict between preferences for large and phenotypically matched groups along a predation risk gradient. We found body-size dependent differences in the resultant social decisions. Large fish preferred shoaling with size-matched individuals, while small fish demonstrated no preference. There was a trend towards reduced preferences for the matched shoal under increased predation risk. Small fish were more active than large fish, moving between shoals more frequently. Activity levels increased as predation risk decreased. We found no effect of unmatched shoal size on preferences or activity.Conclusions and SignificanceOur results suggest that predation risk and individual body size act together to influence shoaling decisions. Oddity was more important for large than small fish, reducing in importance at higher predation risks. Dilution was potentially of limited importance at these shoal sizes. Activity levels may relate to how much sampling of each shoal was needed by the test fish during decision making. Predation pressure may select for better decision makers to survive to larger size, or that older, larger fish have learned to make shoaling decisions more efficiently, and this, combined with their size relative to shoal-mates, and attractiveness as prey items influences shoaling decisions.

Functions of Intermittent Locomotion in Mustached Tamarins (Saguinus mystax)

Many animals interrupt their moving with brief pauses, which appear to serve several different functions. We examined the function of such intermittent locomotion in wild living mustached tamarins (Saguinus mystax), small arboreal New World primates that form mixed-species groups with saddleback tamarins (Saguinus fuscicollis). We investigated how different environmental and social factors affect pausing during locomotion and used these data to infer the function of this behavior. As measures of intermittent locomotion, we used percentage of time spent pausing and pause rate. We considered 3 possible functions that are not mutually exclusive: increased endurance, route planning, and antipredator vigilance. Mustached tamarins spent on average (mean ± SE) 55.1 ± 1.0% of time pausing, which makes effective resource exploitation more time consuming and needs to be outweighed by correspondingly large benefits. Percentage of time spent pausing decreased in larger mixed-species groups vs. smaller mixed-species groups and decreased with height and in monkeys carrying infants. It was not affected by sex, age, spatial arrangement, or single-species group size. Pause rate increased in individuals traveling independently compared to those traveling in file, but was not affected by other factors. The group size effect in mixed-species groups lends support to the notion that pausing during locomotion is an antipredator tactic that can be reduced in the increased safety of larger groups, but other results suggest that additional functions, particularly route planning, are also of great importance. Benefits in terms of predator confusion and group movement coordination are also likely to play a role and remain a topic for further research.

Colour change and assortment in the western rainbowfish

Grouping behaviour is widespread across the animal kingdom, and is known to reduce an individual's risk of predation, for example through predator confusion. Theory predicts that individuals that are different in appearance to the rest of the group are at a greater risk of predation because they are more conspicuous to predators (the ‘oddity’ effect). Thus, animals should choose group mates that are the most similar in appearance to themselves. Another common antipredator tactic is crypsis (camouflage). Fishes are capable of changing colour to match their visual background, but few studies have examined how this might influence shoaling decisions, particularly in the context of the oddity effect. We induced colour pattern changes in a colourful species of freshwater fish, the western rainbowfish, Melanotaenia australis, by maintaining fish in dark and pale aquaria for 2 weeks. Analysis of the proportion of black body pigmentation confirmed that rainbowfish in dark environments developed darker colour patterns than those held in pale environments. We then conducted behavioural observations to determine whether fish subsequently based their shoaling decisions on body coloration. We found that rainbowfish preferred to shoal with similar individuals; fish that had been held in dark aquaria preferred to shoal with other dark fish and fish from pale aquaria preferred other pale fish. Our findings are consistent with the predictions of the oddity effect and demonstrate how morphological colour pattern changes and behavioural decisions interact to mediate antipredator tactics in fish.

Possible functions of the octavolateralis system in fish schooling

AbstractThe development of the octavolateralis system in fish ancestors created the phenomenon of sensory reafference associated with the fish’s own locomotion. Particularly in fish species living and moving in groups, there is a potential to produce complex pressure waves and other water movements interfering with the octavolateralis perception of critical environmental signals. The hypothesis presented is that the development of the octavolateralis system may have initiated, or been a factor in, the evolutionary development of synchronized group locomotion, eventually leading to schooling behaviour. Theoretical models suggest that schooling may be related to a reduction in masking of environmental signals, as well as to survival mechanisms, e.g. confusion of the lateral line and electro‐sensory systems of predators by overlapping pressure waves and overlapping electrical fields. The combined effects of reduced masking and predator confusion may help explain why schooling became an evolutionary success. Including pressure waves and other water movements in the model of join, stay or leave decisions might shed some light on fish shoal assortment. A model encompassing the complex effects of synchronized group locomotion on octavolateralis and electro‐sensory perception of both prey and predator fish might increase the understanding of schooling behaviour.