Spatial relationships and mechanisms of coexistence between dominant and subordinate top predators

Most forest ecosystems contain a diverse community of top‐level predators. How these predator species interact, and how their interactions influence their spatial distribution is still poorly understood. Here we studied interactions among top predators in a guild of diurnal forest raptors in order to test the hypothesis that predation among competing predators (intraguild predation) significantly affects the spatial distribution of predator species, causing subordinate species to nest farther away from the dominant ones. The study analyzed a guild in southwestern Europe comprising three raptor species. For 8 years we studied the spatial distribution of used nests, breeding phenology, intraguild predation, territory occupancy, and nest‐builder species and subsequent nest‐user species. The subordinate species (sparrowhawk Accipiter nisus) nested farther away from the dominant species (goshawk A. gentilis), which preyed on sparrowhawks but not on buzzards Buteo buteo, and closer to buzzards, with which sparrowhawks do not share many common prey. This presumably reflects an effort to seek protection from goshawks. This potential positive effect of buzzards on sparrowhawks may be reciprocal, because buzzards benefit from old sparrowhawk nests, which buzzards used as a base for their nests, and from used sparrowhawk nests, from which buzzards stole prey. Buzzards occasionally occupied old goshawk nests. These results support our initial hypothesis that interspecific interactions within the raptor guild influence the spatial distribution of predator species in forest ecosystems, with intraguild predation as a key driver. We discuss several mechanisms that may promote the coexistence of subordinate and dominant predators and the spatial assembly of this raptor guild: spatial refuges, different breeding phenology, spatial avoidance, low territory occupancy between neighboring nesting territories, nest concealment and protection, and diet segregation.     

Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community

Intraguild predation among natural enemies is common in food webs with insect herbivores at their base. Though intraguild predation may be reciprocal, typically one species suffers more than the other and frequently exhibits behavioural strategies to lessen these effects. How such short-term behaviours influence population dynamics over several generations has been little studied. We worked with a model insect community consisting of two species of aphid feeding on different host plants (Acyrthosiphon pisum on Vicia and Sitobion avenae on Triticum), a parasitoid (Aphidius ervi) that attacks both species, and a dominant intraguild predator (Coccinella septempunctata) that also feeds on both aphids (whether parasitized or not). As reported previously, we found A. ervi avoided chemical traces of C. septempunctata. In population cages in the laboratory, application of C. septempunctata extracts to Vicia plants reduced parasitism on A. pisum. This did not increase parasitism on the other aphid species, our predicted short-term trait-mediated effect. However, a longer term multigenerational consequence of intraguild predator avoidance was observed. In cages where extracts were applied in the first generation of the study, parasitoid recruitment was reduced leading to higher population densities of both aphid species. S. avenae thus benefits from the presence of a dominant intraguild predator foraging on another species of aphid (A. pisum) on a different food plant, a long-term, trait-mediated example of apparent mutualism. The mechanism underlying this effect is hypothesized to be the reduced searching efficiency of a shared parasitoid in the presence of cues associated with the dominant predator.     

Interspecific signalling between mutualists: food-thieving drongos use a cooperative sentinel call to manipulate foraging partners

Interspecific communication is common in nature, particularly between mutualists. However, whether signals evolved for communication with other species, or are in fact conspecific signals eavesdropped upon by partners, is often unclear. Fork-tailed drongos (Dicrurus adsimilis) associate with mixed-species groups and often produce true alarms at predators, whereupon associating species flee to cover, but also false alarms to steal associating species'' food (kleptoparasitism). Despite such deception, associating species respond to drongo non-alarm calls by increasing their foraging and decreasing vigilance. Yet, whether these calls represent interspecific sentinel signals remains unknown. We show that drongos produced a specific sentinel call when foraging with a common associate, the sociable weaver (Philetairus socius), but not when alone. Weavers increased their foraging and decreased vigilance when naturally associating with drongos, and in response to sentinel call playback. Further, drongos sentinel-called more often when weavers were moving, and weavers approached sentinel calls, suggesting a recruitment function. Finally, drongos sentinel-called when weavers fled following false alarms, thereby reducing disruption to weaver foraging time. Results therefore provide evidence of an ‘all clear’ signal that mitigates the cost of inaccurate communication. Our results suggest that drongos enhance exploitation of a foraging mutualist through coevolution of interspecific sentinel signals.     

Association of drongos with myna flocks: Are drongos benefitted?

Common myna(Acridotherus tristis) and jungle myna(Acridotherus fuscus) forage in pure and mixed flocks of various sizes in fallow lands. These flocks were often found associated with drongos that forage individually on the insects herded out by the movements of the flocking myna. We report here the benefits and costs of such association to drongos and mynas. Drongos had a tendency to associate with larger (> 21) than smaller (<20) flocks irrespective of the species composition of the flocks. Drongos associated with larger flocks showed increased foraging trips and harvested more insects in a given time than those that were either isolated or were associated with small flocks. The food range of drongos and mynas differed significantly indicating that they do not compete with each other. Thus our results indicate that drongos are benefitted by this association; however this association neither benefits nor costs to the mynas. The association between the drongos and mynas therefore appears to be commensalistic.     

The influence of hunger,shoal size and predator presence on foraging in bluntnose minnows

This study examines the compromise between predator avoidance and foraging in bluntnose minnows, Pimephales notatus, in shoals of different sizes and at three levels of hunger: 5, 24 or 72 h of deprivation. Trials were carried out in the laboratory with a predator present or absent. Foraging was affected significantly by shoal size, predator presence and hunger. Foraging latency decreased as shoal size and hunger level increased, but latency increased in the presence of a predator. Foraging rate was less when there was a predator present. In the absence of a predator, foraging rate increased as hunger level increased. At the 5 h hunger level, foraging rate increased as shoal size increased, in the absence but not the presence of a predator. At this low level of hunger, innows in all shoal sizes fed at a low rate when the risk of predation was greater. At higher levels of hunger, fish in all shoal sizes fed at a high rate when no predator was present, so that foraging rate did not change across shoal size. When the predator was present at the higher hunger levels, only fish in larger, safer shoals fed at a rate greater than at the lowest hunger level.     

Benefits of Group Foraging Depend on Prey Type in a Small Marine Predator,the Little Penguin

Group foraging provides predators with advantages in over-powering prey larger than themselves or in aggregating small prey for efficient exploitation. For group-living predatory species, cooperative hunting strategies provide inclusive fitness benefits. However, for colonial-breeding predators, the benefit pay-offs of group foraging are less clear due to the potential for intra-specific competition. We used animal-borne cameras to determine the prey types, hunting strategies, and success of little penguins (Eudyptula minor), a small, colonial breeding air-breathing marine predator that has recently been shown to display extensive at-sea foraging associations with conspecifics. Regardless of prey type, little penguins had a higher probability of associating with conspecifics when hunting prey that were aggregated than when prey were solitary. In addition, success was greater when individuals hunted schooling rather than solitary prey. Surprisingly, however, success on schooling prey was similar or greater when individuals hunted on their own than when with conspecifics. These findings suggest individuals may be trading-off the energetic gains of solitary hunting for an increased probability of detecting prey within a spatially and temporally variable prey field by associating with conspecifics.     

Lesser of Two Evils? Foraging Choices in Response to Threats of Predation and Parasitism

Predators have documented post-encounter (density-mediated) effects on prey but their pre-encounter impacts, including behavioural alterations, can be substantial as well. While it is increasingly evident that this “ecology of fear” is important to understand for natural enemy-victim relationships, fear responses of hosts to the threat of infection by a parasite are relatively unknown. We examined larval amphibian (Lithobates pipiens) foraging choices by experimentally manipulating the presence of cues relating to predator (larval odonate) or parasite (the trematode Ribeiroia ondatrae) threats. Tadpoles avoided foraging where predator or parasite cues were present; however, they did not treat these as equal hazards. When both threats were simultaneously present, tadpoles strongly preferred to forage under the threat of parasitism compared to predation, likely driven by their relative lethality in our study. Our results indicate that altered spatial use is an important anti-parasite behaviour, and demonstrate that parasite avoidance can affect foraging in a manner similar to predators, warranting greater study of the pre-encounter effects of this enemy type.     

Relationship between moonlight and nightly activity patterns of the ocelot (Leopardus pardalis) and some of its prey species in Formosa,Northern Argentina

The moon can profoundly influence the activity patterns of animals. If predators are more successful under bright moonlight, prey species are likely to respond by shifting their own activity patterns (predator-avoidance hypothesis). However, the assumption that prey will necessarily avoid full-moon nights does not take into account that moonlight also allows prey to more easily detect predators, and to forage more efficiently. Thus, nightly activity patterns could depend on night vision capabilities (visual-acuity hypothesis). To consider the possible influences of moonlight and to distinguish between these hypotheses, we used camera-trapping records of a predator, the ocelot (Leopardus pardalis), and several of its night-active prey to compare activity patterns under different moonlight conditions. The ocelots' activity patterns were not strongly related to moonlight, but showed a slight tendency for higher activity during brighter nights. Tapeti rabbits (Sylvilagus brasiliensis) and brocket deer (Mazama americana) showed a clear preference for brighter nights. White-eared opossums (Didelphis albiventris) also showed a trend to be less active in new moon light. In contrast, smaller grey four-eyed opossums (Philander opossum) and the poor eye-sight nine-banded armadillo (Dasypus novemcinctus) showed similar activity patterns across all moon phases. Since activity patterns of most prey species were not shifted away from the activity of the ocelot, the differences between species are probably linked to their night vision capabilities, and emphasise the need for more information on the visual system of these taxa. Their activity patterns seem to be less strongly linked to avoidance of predation than previously thought, suggesting that foraging and predator detection benefits may play a more important role than usually acknowledged.     

The presence of an avian co-forager reduces vigilance in a cooperative mammal

Many animals must trade-off anti-predator vigilance with other behaviours. Some species facilitate predator detection by joining mixed-species foraging parties and ‘eavesdropping’ on the predator warnings given by other taxa. Such use of heterospecific warnings presumably reduces the likelihood of predation, but it is unclear whether it also provides wider benefits, by allowing individuals to reduce their own vigilance. We examine whether the presence of an avian co-forager, the fork-tailed drongo (Dicrurus adsimilis), affects rates of vigilance (including sentinel behaviour) in wild dwarf mongooses (Helogale parvula). We simulate the presence of drongos—using playbacks of their non-alarm vocalizations—to show that dwarf mongooses significantly reduce their rate of vigilance when foraging with this species. This is, to our knowledge, the first study to demonstrate experimentally that a mammal reduces vigilance in the presence of an avian co-forager.     

Population and behavioural responses of native prey to alien predation

The introduction of invasive alien predators often has catastrophic effects on populations of naïve native prey, but in situations where prey survive the initial impact a predator may act as a strong selective agent for prey that can discriminate and avoid it. Using two common species of Australian small mammals that have persisted in the presence of an alien predator, the European red fox Vulpes vulpes, for over a century, we hypothesised that populations of both would perform better where the activity of the predator was low than where it was high and that prey individuals would avoid signs of the predator’s presence. We found no difference in prey abundance in sites with high and low fox activity, but survival of one species—the bush rat Rattus fuscipes—was almost twofold higher where fox activity was low. Juvenile, but not adult rats, avoided fox odour on traps, as did individuals of the second prey species, the brown antechinus, Antechinus stuartii. Both species also showed reduced activity at foraging trays bearing fox odour in giving-up density (GUD) experiments, although GUDs and avoidance of fox odour declined over time. Young rats avoided fox odour more strongly where fox activity was high than where it was low, but neither adult R. fuscipes nor A. stuartii responded differently to different levels of fox activity. Conservation managers often attempt to eliminate alien predators or to protect predator-naïve prey in protected reserves. Our results suggest that, if predator pressure can be reduced, otherwise susceptible prey may survive the initial impact of an alien predator, and experience selection to discriminate cues to its presence and avoid it over the longer term. Although predator reduction is often feasible, identifying the level of reduction that will conserve prey and allow selection for avoidance remains an important challenge.     

Variation of prey responses to cues from a mesopredator and an apex predator

Detection and avoidance of predator cues can be costly, so it is important for prey to balance the benefits of gaining food against the costs of avoiding predators. Balancing these factors becomes more complicated when prey are threatened by more than one type of predator. Hence, the ability to recognize species‐specific predator odours and prioritize behaviours according to the level of risk is essential for survival. We investigated how rock rats, Zyzomys spp. modify their foraging behaviour and giving‐up density (GUD) in the presence of an apex predator, the dingo Canis dingo, a mesopredator, the northern quoll Dasyurus hallucatus, a herbivore, the rock wallaby Petrogale brachyotis as a pungency control and water as a procedural control. Both dingoes and quolls consume rock rats, but because quolls can enter small crevices inhabited by rock rats, they pose a greater threat to rock rats than dingoes. Rock rats demonstrated a stronger avoidance to quoll odour than dingo odour, and no avoidance of the pungency control (rock wallaby) and the procedural control (water). GUD values declined significantly over the duration of the study, but did not differ between odour treatments. Our results support the hypothesis that prey vary behaviour according to perceived predator threat, and show stronger responses to potentially more dangerous predators.     

Does an opportunistic predator preferentially attack nonvigilant prey?

The dilution effect as an antipredation behaviour is the main theoretical reason for grouping in animals and states that all individuals in a group have an equal risk of being predated if equally spaced from each other and the predator. Stalking predators, however, increase their chance of attack success by preferentially targeting nonvigilant individuals, potentially making relative vigilance rates in a group relatively important in determining predation compared with the dilution effect. Many predators, however, attack opportunistically without stalking, when targeting of nonvigilant individuals may be less likely, so that the dilution effect will then be a relatively more important antipredation reason for grouping. We tested whether an opportunistically hunting predator, the sparrowhawk, Accipiter nisus, preferentially attacked vigilant or feeding prey models presented in pairs. We found that sparrowhawks attacked vigilant and feeding mounts at similar frequencies. Our results suggest that individuals should prioritize maximizing group size or individual vigilance dependent on the type of predator from which they are at risk. When the most likely predator is a stalker, individuals should aim to have the highest vigilance levels in a group, and there may be relatively little selective advantage to being in the largest group. In contrast, if the most likely predator is an opportunist, then individuals should simply aim to be in the largest group and can also spend more time foraging without compromising predation risk. For most natural systems this will mean a trade-off between the two strategies dependent on the frequency of attack of each predator type. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.     

The effects of predator presence and shoal size on foraging in bluntnose minnows,Pimephales notatus

Synopsis Shoals of 3, 5, 7, 10, 15, and 20 bluntnose minnows,Pimephales notatus, were allowed to forage in the absence and presence of a fish predator, which was separated from the shoal by a clear plexiglass partition. A typical dilution effect was observed in that individual fish in larger shoals were approached less frequently by the predator. In the absence of a predator, foraging latency decreased significantly and the rate of foraging increased with increasing shoal size. Foraging latency for each shoal size tended to increase in the presence of a predator and foraging rate decreased, significantly for shoals of 7, 15, and 20 fish. Members of larger shoals were safer and enjoyed a greater level of food consumption, perhaps due to decreased individual vigilance for predators and social facilitation. However, foraging effort decreased when a predator was present, as more time was allocated to predator avoidance.     

Behavioral Response of Corophium volutator to Shorebird Predation in the Upper Bay of Fundy,Canada

Predator avoidance is an important component of predator-prey relationships and can affect prey availability for foraging animals. Each summer, the burrow-dwelling amphipod Corophium volutator is heavily preyed upon by Semipalmated Sandpipers (Calidris pusilla) on mudflats in the upper Bay of Fundy, Canada. We conducted three complementary studies to determine if adult C. volutator exhibit predator avoidance behavior in the presence of sandpipers. In a field experiment, we monitored vertical distribution of C. volutator adults in bird exclosures and adjacent control plots before sandpipers arrived and during their stopover. We also made polymer resin casts of C. volutator burrows in the field throughout the summer. Finally, we simulated shorebird pecking in a lab experiment and observed C. volutator behavior in their burrows. C. volutator adults were generally distributed deeper in the sediment later in the summer (after sandpipers arrived). In August, this response was detectably stronger in areas exposed to bird predation than in bird exclosures. During peak predator abundance, many C. volutator adults were beyond the reach of feeding sandpipers (>1.5 cm deep). However, burrow depth did not change significantly throughout the summer. Detailed behavioral observations indicated that C. volutator spent more time at the bottom of their burrow when exposed to a simulated predator compared to controls. This observed redistribution suggests that C. volutator adults move deeper into their burrows as an anti-predator response to the presence of sandpipers. This work has implications for predators that feed on burrow-dwelling invertebrates in soft-sediment ecosystems, as density may not accurately estimate prey availability.     

Effects of size,caudal autotomy,and predator kairomones on the foraging behavior of Allegheny Mountain dusky salamanders (<Emphasis Type="Italic">Desmognathus ochrophaeus</Emphasis>)

Prey must balance the conflicting demands of foraging and defensive behavior. Foraging under the threat of predation may be further complicated among species that engage in caudal autotomy, the loss of a portion of the tail at preformed breakage planes, because the tail may serve as an important energy storage organ and contribute to motility, culminating in a trade-off between foraging and predator avoidance. As a result of the advantages conferred by the presence of a tail, individuals that have recently undergone autotomy may be more motivated to forage despite elevated levels of threat indicated by predator kairomones. We used a full factorial design to evaluate the combined effects of body size, exposure to predator kairomones, and experience with autotomy on the latency to strike at Drosophila prey, number of strikes, and prey captured per strike by Allegheny Mountain dusky salamanders (Desmognathus ochrophaeus). In our study, caudal autotomy was the only significant main effect and influenced both the latency to attack prey and the number of strikes attempted. In terms of latency to attack prey, there was a significant interaction between body size and autotomy such that “small” salamanders (≤3.2 cm SVL) without tails delayed their foraging behavior. In terms of the number of strikes toward prey, there was a significant interaction between autotomy and exposure to predator kairomones such that individuals with intact tails exhibited a greater number of strikes, with the exception of the “large” (>3.2 cm SVL) salamanders, which performed fewer strikes when exposed to the snake kairomones. There was no significant effect on foraging efficiency, although the trend in the data suggests that autotomized individuals forage more efficiently. This study was designed to evaluate the confluence of factors related to size, caudal autotomy, and exposure to stimuli from predators and hints at the magnitude of caudal autotomy on antipredator decision-making. Our data suggest that despite the importance of tail tissue for energy storage, locomotion, and mating, salamanders without tails are cautious when foraging under elevated risk.     

Birds at the Winter Feeder do not Recognize an Artificially Coloured Predator

It is supposed that coloration may affect the recognition of predators by prey species; nevertheless, the significance of the coloration and its particular components in the recognition process remains unknown. We presented dummies of the European sparrowhawk (Accipiter nisus) with changed body coloration, but with all other typical features preserved (body size and shape, beak, eyes, legs), to great tits (Parus major) and blue tits (Cyanistes caeruleus) visiting a winter feeder. A pigeon (Columba livia f. domestica) dummy was used as a harmless control. Neither tit species showed passive avoidance in the presence of a dummy with an artificial, violet‐white chequered coloration. They obviously did not consider such an object to be a predator despite the presence of the raptor beak, eyes and talons. Sparrowhawk dummies with the coloration completely changed (altered with those of a harmless European robin) or with the typical colour feature removed (barred pattern on the underparts) were considered to be as dangerous as the unmodified sparrowhawk. We discuss the possibility that the effect of salient raptor‐like features such as beak shape, eye coloration, and leg and talons shape overwhelmed the effect of body coloration in these cases. Birds visiting the feeder probably were able to generalize the vigilance towards the sparrowhawk to other realistically coloured dummies, but not to the non‐natural dummy.     

Seeing is believing: information content and behavioural response to visual and chemical cues

Predator avoidance and foraging often pose conflicting demands. Animals can decrease mortality risk searching for predators, but searching decreases foraging time and hence intake. We used this principle to investigate how prey should use information to detect, assess and respond to predation risk from an optimal foraging perspective. A mathematical model showed that solitary bees should increase flower examination time in response to predator cues and that the rate of false alarms should be negatively correlated with the relative value of the flower explored. The predatory ant, Oecophylla smaragdina, and the harmless ant, Polyrhachis dives, differ in the profile of volatiles they emit and in their visual appearance. As predicted, the solitary bee Nomia strigata spent more time examining virgin flowers in presence of predator cues than in their absence. Furthermore, the proportion of flowers rejected decreased from morning to noon, as the relative value of virgin flowers increased. In addition, bees responded differently to visual and chemical cues. While chemical cues induced bees to search around flowers, bees detecting visual cues hovered in front of them. These strategies may allow prey to identify the nature of visual cues and to locate the source of chemical cues.     

An ambusher's arsenal: chemical crypsis in the puff adder (Bitis arietans)

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.     

Common ravens, Corvus corax, preferentially associate with grey wolves, Canis lupus, as a foraging strategy in winter

One foraging strategy that scavengers can employ to discover unpredictable food sources is to associate directly with predators who inadvertently provide food. The common raven, a well known feeding generalist, is also a prominent scavenger of wolves' kills and is found to be in close association with this predator. We tested the hypothesis that ravens preferentially associate with wolves in winter as a kleptoparasitic foraging strategy. The presence, absence and behaviour of ravens was documented during winter observations of wolves, coyotes, Canis latrans, and elk, Cervus elaphus, as well as the landscape in the absence of these three species. Ravens were found to be in close association with wolves when they were travelling, resting and hunting prey. In comparison, ravens showed no significant association with coyotes, elk or areas on the landscape in the absence of wolves. We also compared ravens' discovery success of wolf-killed and nonwolf-killed carcasses and their behavioural response upon discovery. Ravens found all wolf kills almost immediately and remained at the carcass to feed alongside wolves after the death of the prey. In contrast, ravens were less successful discovering experimentally placed carcasses in the same study region, and did not land or feed despite the availability of fresh, exposed meat. Our results show that ravens' association with wolves is not just an incidental and proximate by-product of the presence of fresh meat. Instead, we show that ravens preferentially associate with wolves in both the presence and absence of food, resulting in the discovery of carcasses and suppression of ravens' innate fear of novel food sources. Through this mode of social foraging, ravens may experience increased foraging efficiency in the use of an otherwise spatially and temporally unpredictable food source.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Foraging decisions of North American beaver (<Emphasis Type="Italic">Castor canadensis</Emphasis>) are shaped by energy constraints and predation risk

Foraging herbivores have to trade-off between energy requirements and predator avoidance. We aimed to study the relative roles of these factors in beavers (Castor canadensis) when foraging on land. We hypothesized that beavers were able to assess the risk of predation by using two main cues: the distance from the water and the presence or absence of predator odors. First, we studied the food selection of beavers in relation to distance from the water in natural settings. The transects were made at beaver ponds, and the diameter, species, and distance from the shore of intact and beaver-cut trees were recorded. Secondly, we placed rows of aspen sticks (Populus tremula) perpendicular to the shore around beaver ponds, and treated each row with a neutral, alien, or wolf odor. We found that aspen, downy birch (Betula pubescens), and speckled alder (Alnus incana) were the preferred tree species. More of these species were cut close to the shore, and cut trees were smaller further away from the shore, except in the case of aspen. In the experiment, most of the aspen sticks were taken close to the shore. As predicted, beavers took less aspen sticks in rows treated with wolf odor than water. As the predator odor did not affect the foraging distance from the shore, it is likely that our observation that foraging was the most intense close to shore is due to energetic constraints. However, predation risk probably affects the decision whether to forage on the land in the first place.