Fear of humans as apex predators has landscape‐scale impacts from mountain lions to mice

Apex predators such as large carnivores can have cascading, landscape‐scale impacts across wildlife communities, which could result largely from the fear they inspire, although this has yet to be experimentally demonstrated. Humans have supplanted large carnivores as apex predators in many systems, and similarly pervasive impacts may now result from fear of the human ‘super predator’. We conducted a landscape‐scale playback experiment demonstrating that the sound of humans speaking generates a landscape of fear with pervasive effects across wildlife communities. Large carnivores avoided human voices and moved more cautiously when hearing humans, while medium‐sized carnivores became more elusive and reduced foraging. Small mammals evidently benefited, increasing habitat use and foraging. Thus, just the sound of a predator can have landscape‐scale effects at multiple trophic levels. Our results indicate that many of the globally observed impacts on wildlife attributed to anthropogenic activity may be explained by fear of humans.     

Perception of alarm cues influences the outcome of shelter competition in crayfish20

The effects of predators on prey populations may significantly alter many aspects of prey biology, including spatial distribution, foraging activities, and social interactions. In aquatic habitats, chemosensation is an important mode of communication and has been shown for many taxa, including crayfish, to be used in detection of predator and/or conspecific alarm cues. Here, we report on an experiment to test the hypothesis that detection of alarm cues results in greater individual investment in contests over shelters. We tested this hypothesis through dyadic contests between sex- and size-matched, non-reproductive individuals of Faxonius virilis. We found that crayfish responded to exposure to alarm cues by spending more time inside a shelter. We also report that in contests between pairs in which one crayfish had been exposed to alarm cues and the other had not, exposed individuals were significantly more likely to win ownership of a single shelter. However, we did not detect any differences in the contest parameters we recorded between exposed and unexposed crayfish. These impacts on both individual and social behavior indicate that the presence of predators is likely to have large effects on the distribution and structure of crayfish populations.     

The evolution of vocal alarm communication in rodents

On encountering a predator, many species emit potentially riskyvocalizations known as alarm calls. We evaluated the relativeimportance of two adaptive hypotheses on the evolution of calling:(1) communicating to predators, which may function by deterringpursuit and hence increasing individual survival, and (2) analternative nepotistic hypothesis for alarm calling wherebycallers obtain direct and indirect fitness by warning relatives.Focusing on 209 species of rodents, we found significant associationsbetween diurnality and alarm calling, living socially and alarmcalling, and diurnality and sociality. Diurnality, however,accounted for nearly three times as much variation in whetheror not a species alarm called than did sociality. Phylogenetictests revealed that the evolution of diurnality preceded theevolution of alarm calling, and that the evolutions of diurnalityand sociality were unrelated. Our results are consistent withthe hypothesis that alarm communication evolved to communicateto predators. If so, then nepotistic benefits, although importantfor the maintenance of alarm calling in some rodents, may berelatively less important in its evolution.     

The Sound of Arousal: The Addition of Novel Non-linearities Increases Responsiveness in Marmot Alarm Calls

Vocal structure should reflect vocal function. While much attention has focused on quantifying attributes of harmonic vocalizations, the vocalizations of many species also may contain non-linear phenomena such as warbles, subharmonics, biphonation, and deterministic chaos or noise. The function of these non-linearities remains enigmatic. In some species, harmonic vocalizations abruptly become 'noisy' when individuals are physiologically aroused and the sudden onset of these non-linearities could signal arousal or fear to receivers. One untested functional hypothesis is that vocalizations containing non-linearities are more variable from one rendition to the next, and thus are harder to habituate to. In some situations, reducing the likelihood of habituation could be important. Signals that are highly evocative are more difficult to habituate to. Thus, we conducted playback experiments to foraging yellow-bellied marmots ( Marmota flaviventris ) to determine whether the addition of white noise (a non-linear acoustic phenomenon) to alarm calls elicited a greater response than control calls without the non-linearity or control calls with silence, rather than noise, added to them. Marmots spent less time foraging after hearing calls that included noise than after normal or control calls. This result is consistent with the unpredictability hypothesis and suggests that the adaptive value of non-linearities is to prevent habituation.     

Interspecific audience effects on the alarm-calling behaviour of a kleptoparasitic bird

Audience effects are increasingly recognized as an important aspect of intraspecific communication. Yet despite the common occurrence of interspecific interactions and considerable evidence that individuals respond to the calls of heterospecifics, empirical evidence for interspecific audience effects on signalling behaviour is lacking. Here we present evidence of an interspecific audience effect on the alarm-calling behaviour of the kleptoparasitic fork-tailed drongo (Dicrurus adsimilis). When foraging solitarily, drongos regularly alarm at aerial predators, but rarely alarm at terrestrial predators. In contrast, when drongos are following terrestrially foraging pied babblers (Turdoides bicolor) for kleptoparasitic opportunities, they consistently give alarm calls to both aerial and terrestrial predators. This change occurs despite no difference in the amount of time that drongos spend foraging terrestrially. Babblers respond to drongo alarm calls by fleeing to cover, providing drongos with opportunities to steal babbler food items by occasionally giving false alarm calls. This provides an example of an interspecific audience effect on alarm-calling behaviour that may be explained by the benefits received from audience response.     

Possible use of heterospecific food-associated calls of macaques by sika deer for foraging efficiency

Heterospecific communication signals sometimes convey relevant information for animal survival. For example, animals use or eavesdrop on heterospecific alarm calls concerning common predators. Indeed, most observations have been reported regarding anti-predator strategies. Use of heterospecific signals has rarely been observed as part of a foraging strategy. Here, I report empirical evidence, collected using playback experiments, showing that Japanese sika deer, Cevus nippon, use heterospecific food calls of Japanese macaques, Macaca fuscata yakui, for foraging efficiency. The deer and macaques both inhabit the wild forest of Yakushima Island with high population densities and share many food items. Anecdotal observations suggest that deer often wait to browse fruit falls under the tree where a macaque group is foraging. Furthermore, macaques frequently produce food calls during their foraging. If deer effectively obtain fruit from the leftovers of macaques, browsing fruit fall would provide a potential benefit to the deer, and, further, deer are likely to associate macaque food calls with feeding activity. The results showed that playback of macaque food calls under trees gathered significantly more deer than silence control periods. These results suggest that deer can associate macaque food calls with foraging activities and use heterospecific calls for foraging efficiency.     

The Predator Deterrence Function of Primate Alarm Calls

It is generally assumed that alarm calls function in intraspecific communication, for example to warn close relatives about the presence of a predator. However, an alternative hypothesis suggests that, in some cases, signallers may also gain fitness benefits in directly communicating to the predator, for example by advertising perception and unprofitability to predators that depend on unprepared prey. In this study, we show that six monkey species in Taï forest, Ivory Coast, produce significantly more alarm calls to leopards than to chimpanzees, although both are notorious monkey predators. The conspicuously high vocalization rates to leopards had adaptive consequences for the monkeys. By following a radio-collared leopard, we found that after detection and high alarm call rates the leopard gave up its hiding location and left the group significantly faster than would be expected by chance. We discuss these data with respect to the various functional hypothesis of alarm call behaviour and conclude that the high alarm call rates to leopards are part of an anti-predator strategy in primates that may have evolved to deter predators that depend on surprise.     

High Concentrations of the Alarm Pheromone Component,Isopentyl Acetate,Reduces Foraging and Dancing in <Emphasis Type="Italic">Apis mellifera</Emphasis> Ligustica and <Emphasis Type="Italic">Apis cerana</Emphasis> Cerana

A honeybee colony is a superorganism that has evolved precise communication systems, which allow the colony to gather information from numerous individuals and coordinate its behavior. Alarm pheromones, such as isopentyl acetate (IPA), the main component of sting alarm pheromone, play a critical role in the coordination of individual behaviors as well as colony communication in honeybee colonies. In this study, honeybees (Apis mellifera ligustica and Apis cerana cerana) were exposed to relatively high levels of IPA at a foraging site (6–8 bee equivalents) and inside their colony (28–58 bee equivalents) to investigate the influence of alarm pheromones on foraging activity and hive flight activity. IPA reduced the number of bees that flew out the hive, foraged, and waggle danced. Under both contexts in the hive and at the food source, IPA can therefore inhibit honey bee foraging and foraging communication.     

Anti‐Predator Signals in the Chaffinch Fringilla coelebs in Response to Habitat Structure and Different Predator Types

Many animals respond to the presence of predators with conspicuous signals such as alarm calling. These signals may aid the detection of the predator by conspecifics or may deter the predator from attack. The advantages of such signals may be dependent upon predator type and habitat type. We measured signalling behaviours (alarm calling and tail flicking) in foraging chaffinches in response to different predator models (hawk and pigeon control, cat and plastic box as control). In addition we measured responses to a cat model when chaffinches were foraging in different habitat structures (obstructed vs. open). There was no difference in the number of individual chaffinches alarm calling in obstructed vs. open habitat, but birds tail flicked more in open habitat, suggesting that tail flicking acts as a visual signal to the predator or conspecifics and therefore unlike auditory cues is influenced by habitat structure. Chaffinches were also more likely to tail flick in response to the cat model than the other three models. Our results are consistent with the idea that animals may respond to ground predators, which spend a large amount of time observing prey before attack, by using signalling behaviours, such as tail flicking and alarm calling. Further work on prey selection by predators is needed to separate the functions of signalling behaviour in response to predators.     

Trophic rewilding establishes a landscape of fear: Tasmanian devil introduction increases risk‐sensitive foraging in a key prey species

Global declines of large carnivores have reduced the ‘landscape of fear’ that constrains the behaviour of other species. In recent years, active and passive trophic rewilding have potentially begun restoring these lost top–down controls. The Tasmanian devil Sarcophilus harrisii has declined severely due to a novel transmissible cancer. In response to extinction fears, devils were introduced to the devil‐free Maria Island, where their abundance rapidly increased. We tested how this introduction influenced risk‐sensitive foraging in the common brushtail possum Trichosurus vulpecula, a major prey species for devils, using giving‐up densities (GUDs). Before the introduction of devils, possum GUDs on Maria Island were indistinguishable from the long‐diseased region of Tasmania, where devils have been rare since ~2000. Three years after devil introduction, GUDs were 64% higher on Maria Island than the control region, demonstrating that after an initial period of high mortality, possums quickly adopted risk‐sensitive foraging behaviours. Devil activity across Maria Island was variable, leading to a heterogeneous landscape of fear and highlighting that top predators must be at functional densities to elicit behavioural responses from prey. Our study provides strong evidence that top predators modify the behaviour of prey by instilling fear, causing rapid ecological change following recoveries.     

Top carnivores increase their kill rates on prey as a response to human-induced fear

The fear induced by predators on their prey is well known to cause behavioural adjustments by prey that can ripple through food webs. Little is known, however, about the analogous impacts of humans as perceived top predators on the foraging behaviour of carnivores. Here, we investigate the influence of human-induced fear on puma foraging behaviour using location and prey consumption data from 30 tagged individuals living along a gradient of human development. We observed strong behavioural responses by female pumas to human development, whereby their fidelity to kill sites and overall consumption time of prey declined with increasing housing density by 36 and 42%, respectively. Females responded to this decline in prey consumption time by increasing the number of deer they killed in high housing density areas by 36% over what they killed in areas with little residential development. The loss of food from declines in prey consumption time paired with increases in energetic costs associated with killing more prey may have consequences for puma populations, particularly with regard to reproductive success. In addition, greater carcass availability is likely to alter community dynamics by augmenting food resources for scavengers. In light of the extensive and growing impact of habitat modification, our study emphasizes that knowledge of the indirect effects of human activity on animal behaviour is a necessary component in understanding anthropogenic impacts on community dynamics and food web function.     

An asymmetric producer-scrounger game: body size and the social foraging behavior of coho salmon

A tension between cooperation and conflict characterizes the behavioral dynamics of many social species. The foraging benefits of group living include increased efficiency and reduced need for vigilance, but social foraging can also encourage theft of captured prey from conspecifics. The payoffs of stealing prey from others (scrounging) versus capturing prey (producing) may depend not only on the frequency of each foraging strategy in the group but also on an individual’s ability to steal. By observing the foraging behavior of juvenile coho salmon (Oncorhynchus kisutch), we found that, within a group, relatively smaller coho acted primarily as producers and took longer to handle prey, and were therefore more likely to be targeted by scroungers than relatively larger coho. Further, our observations suggest that the frequency of scrounging may be higher when groups contained individuals of different sizes. Based on these observations, we developed a model of phenotype-limited producer-scrounger dynamics, in which rates of stealing were structured by the relative size of producers and scroungers within the foraging group. Model simulations show that when the success of stealing is positively related to body size, relatively large predators should tend to be scroungers while smaller predators should be producers. Contrary to previous models, we also found that, under certain conditions, producer and scrounger strategies could coexist for both large and small phenotypes. Large scroungers tended to receive the highest payoff, suggesting that producer-scrounger dynamics may result in an uneven distribution of benefits among group members that—under the right conditions—could entrench social positions of dominance.     

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.     

On the Meaning of Alarm Calls: A Review of Functional Reference in Avian Alarm Calling

A long‐standing question in animal communication is whether signals reveal intrinsic properties of the signaller or extrinsic properties of its environment. Alarm calls, one of the most conspicuous components of antipredator behaviour, intuitively would appear to reflect internal states of the signaller. Pioneering research in primates and fowl, however, demonstrated that signallers may produce unique alarm calls during encounters with different types of predators, suggesting that signallers through selective production of alarm calls provide to conspecific receivers information about predators in the environment. In this article, we review evidence for such ‘functional reference’ in the alarm calls of birds based on explicit tests of two criteria proposed in Macedonia & Evans’ (Ethology 93, 1993, 177) influential conceptual framework: (1) that unique alarm calls are given to specific predator categories, and (2) that alarm calls isolated from contextual information elicit antipredator responses from receivers similar to those produced during actual predator encounters. Despite the importance of research on birds in development of the conceptual framework and the ubiquity of alarm calls in birds, evidence for functionally referential alarm calls in this clade is limited to six species. In these species, alarm calls are associated with the type of predator encountered as well as variation in hunting behaviour; with defence of reproductive effort in addition to predators of adults; with age‐related changes in predation risk; and with strong fitness benefits. Our review likely underestimates the occurrence of functional reference in avian alarm calls, as incomplete application and testing of the conceptual framework has limited our understanding. Throughout, therefore, we suggest avian taxa for future studies, as well as additional questions and experimental approaches that would strengthen our understanding of the meaning of functional reference in avian alarm calls.     

Vigilance and Collective Detection of Predators in Degus (Octodon degus)

Individuals of social and partially social species typically reduce their vigilance activity when foraging in groups. As a result, per capita risk of predation decreases and individuals allocate more time to foraging and other fitness rewarding activities. Reduction of per capita risk is hypothesized to occur because there are more individuals to detect potential predators. If so, collective (i.e. total) vigilance is expected to increase with foraging group size. Increased surveillance during group foraging may occur if group members scan independently of one another, or sequentially to avoid the overlapping of their vigilance bouts. Intriguingly, such coordinated vigilance assumes that individuals monitor not only the presence, but the vigilance behaviour of group mates. We used seasonal records on time budget and grouping patterns of individually marked degus (Octodon degus), a social rodent, to examine if (a) individual vigilance decreases and/or foraging increases with group size, (b) collective vigilance increases with group size and (c) foraging degus coordinate their vigilance. When foraging, degus decreased their individual vigilance and increased their foraging time when in larger groups. Despite this, degus in larger groups increased their collective vigilance, supporting the hypothesis that socially foraging degus decrease predation risk through an improved ability to detect and escape potential predators. Additionally, patterns of collective vigilance suggested that degus scan independently of each other and so, they do not coordinate their vigilance to prevent its temporal overlapping. This finding does not support that foraging degus monitor the vigilance activity of group mates.     

The jellyfish buffet: jellyfish enhance seabird foraging opportunities by concentrating prey

High levels of jellyfish biomass have been reported in marine ecosystems around the world, but understanding of their ecological role remains in its infancy. Jellyfish are generally thought to have indirect negative impacts on higher trophic-level predators, through changes in lower trophic pathways. However, high densities of jellyfish in the water column may affect the foraging behaviour of marine predators more directly, and the effects may not always be negative. Here, we present novel observations of a diving seabird, the thick-billed murre, feeding on fish aggregating among the long tentacles of large jellyfish, by using small video loggers attached to the birds. We show that the birds encountered large jellyfish, Chrysaora melanaster, during most of their dives, commonly fed on fish associated with jellyfish, and appeared to specifically target jellyfish with a high number of fish aggregating in their tentacles, suggesting the use of jellyfish may provide significant energetic benefits to foraging murres. We conclude that jellyfish provide feeding opportunities for diving seabirds by concentrating forage fish, and that the impacts of jellyfish on marine ecosystems are more complex than previously anticipated and may be beneficial to seabirds.     

Anthropogenic noise reduces avian feeding efficiency and increases vigilance along an urban–rural gradient regardless of species’ tolerances to urbanisation

Anthropogenic noise can adversely impact urban bird populations by interfering with vocal communication. Less research has addressed if anthropogenic noise masks the adventitious sounds that birds use to aid predator detection, which may lead to increased vigilance and reduced feeding efficiency. We test this hypothesis using a controlled playback experiment along an urban–rural gradient in Sheffield (UK). We also test the related predictions that anthropogenic noise has the greatest impacts on vigilance and feeding efficiency in rural populations, and on species that are more sensitive to urbanisation. We focus on six passerines, in order from most to least urbanised (based on how urbanisation influences population densities): blue tit Cyanistes caeruleus, robin Erithacus rubeculla, great tit Parus major, chaffinch Fringilla coelebs, coal tit Periparus ater and nuthatch Sitta europaea. We used play-back of anthropogenic urban noise and a control treatment at 46 feeding stations located along the urban–rural gradient. We assess impacts on willingness to visit feeders, feeding and vigilance rates. Exposure to anthropogenic noise reduced visit rates to supplementary feeding stations, reduced feeding rates and increased vigilance. Birds at more urban sites exhibit less marked treatment induced reductions in feeding rates, suggesting that urban populations may be partially habituated or adapted to noisy environments. There was no evidence, however, that more urbanised species were less sensitive to the impacts of noise on any response variable. Our results support the adventitious sound masking hypothesis. Urban noise may thus interfere with the ability of birds to detect predators, reducing their willingness to use food rich environments and increase vigilance rates resulting in reduced feeding rates. These adverse impacts may compromise the quality of otherwise suitable foraging habitats in noisy urban areas. They are likely to be widespread as they arise in a range of species including common urban birds.     

Predator Avoidance and Alarm-response Behaviour in Kin-discriminating Tadpoles (Rana cascadae)

When captured by predators, the tadpoles of some species of frogs and toads may release an alarm substance that alters the behaviour of conspecifics. Such ‘alarm response’ behaviour has been proposed as a potential mechanism whereby related conspecifics may ‘warn’ relatives of a predator's presence and thus, improve their inclusive fitness. We examined predator avoidance and alarm response behaviour in tadpoles of the Cascades frog (Rana cascadae) and tested whether such behaviour is influenced by kinship factors. Tadpoles reduced activity when in the presence of a predatory newt (Taricha granulosa). Individuals in sibling groups were more active than both solitary tadpoles and individuals in mixed groups of siblings and nonsiblings. However, we found no evidence of an alarm response in R. cascadae. Behaviour of tadpoles in groups exposed only to predators was not different from that of tadpoles in groups exposed to predators plus crushed conspecifics. Tadpoles in groups exposed to crushed tadpoles were as active as tadpoles in groups exposed to water controls, and some test individuals fed upon the dead tadpoles. Thus, while R. cascadae tadpoles reduce activity in response to newt predators, crushed tadpoles appear to initiate a feeding response rather than an alarm response as has been previously proposed.     

Scaling from plot experiments to landscapes: studying grasshoppers to inform forest ecosystem management

Ecologists studying food web interactions routinely conduct their experiments at scales of 1–10 m² whereas real-world landscape-level management problems exist on scales of 10⁶ m² or larger. It is often asserted that the experimental tradition in ecology has little to offer to environmental management because small scale empirical insights are not easily, if at all, translatable to the large scale problems. Small scale experiments are very local in nature and they are conducted in ways that tend to homogenize background environmental variation. Real world management is conducted across vast landscapes. Managers routinely must wrestle with complexity that is introduced by the heterogeneous structure of those landscapes and they often have limited recourse to do careful experimentation. How then is empirical ecological science ever to inform landscape-level management? The solution to this dilemma lies in arriving at good working conceptualizations of ecosystem structure and function that embody principles that are relatively scale independent. In this paper, the evolutionary ecological principle of foraging versus predation risk avoidance trade-offs is proffered as one central organizing conceptualization for plant-herbivore interactions across all systems. The utility of this conceptualization is first illustrated by presenting results of detailed experiments involving spider predators, grasshopper herbivores, and two classes of plant resources that afford grasshoppers differential protection from predators: nutritionally superior but risky grasses and less nutritious but safer herbs. The paper then shows how the foraging versus predation risk avoidance conceptualization in the context of a “landscape of fear” can be applied to manage large herbivore impacts of forest regeneration following forest harvesting. I present results of landscape-scale experiments that mediate predation risk of the herbivores through manipulation of safe habitat in order to enlist herbivores to facilitate boreal forest mixed species regeneration through preferential foraging of certain woody species.     

Predation risk in tadpole populations shapes behavioural responses of prey but not strength of trait‐mediated indirect interactions

Prey animals often respond to predators by reducing activity levels. This can produce a trait‐mediated indirect interaction (TMII) between predators and prey resources, whereby reduced foraging by prey in the presence of a predator causes an increase in prey resources. TMIIs play important roles in structuring communities, and it is important to understand factors that determine their strength. One such influence may be behavioural variation in the prey species, with indirect effects of predators being stronger within populations that are more responsive to the presence of a predator. We tested 1) whether the behavioural responsiveness of populations of wood frog tadpoles to predator cues was related to the predation risk in their native ponds, and 2) whether more responsive tadpoles yielded stronger TMIIs. To do this, we 1) measured the activity of tadpoles from 18 populations in mesocosms with and without caged predators, and 2) measured changes in the biomass of periphyton (the tadpoles’ diet) between predator treatments for each population. We found that tadpoles from higher predation risk ponds reduced their time outside refuges more in the presence of predators and tended to move less when visible, suggesting possible local adaptation to predation regimes. Though the presence of predators generally resulted in higher periphyton biomass – a TMII – there was no evidence that the strength of this TMII was affected by variation in tadpole behaviour. Foraging activity and general activity may be decoupled to some extent, enabling high predation risk‐adapted tadpoles to limit the fitness costs of reduced foraging when predators are present.