When the Ghost of Predation has Passed: Do Rodents from Islands with and without Fox Predators Exhibit Aversion to Fox Cues?

Anti‐predator behavior can alter the dynamics of prey populations, but little is known about the rate at which anti‐predator behavior is lost from prey populations following predator removal. The Channel Islands differ in whether they have historically contained a top predator, the Island Fox (Urocyon littoralis), in evolutionary time (approximately 6200–10 000 yr). On a historically fox‐containing island and two historically fox‐free islands in 2007, I deployed live traps that contained olfactory cues of fox predators (fox feces), olfactory cues of an herbivore (horse feces) or a no‐feces control. Due to a captive breeding program, foxes on the historically fox‐containing island were effectively removed from 1998 to 2004. Rodents from one of the historically fox‐free islands did not respond to fox cues, whereas rodents on the historically fox‐containing island were more likely to be captured in a control trap and less likely to be captured in a fox‐cue trap. Results from the other historically fox‐free island that experienced a recent population bottleneck and period of captive rearing exhibited a preference for horse‐scented traps. These results suggest that, on islands where foxes are the primary predators, anti‐predator behavior in response to olfactory cues is not likely to be rapidly lost by short‐term removals of foxes, although the nature of anti‐predator behavior may depend upon founder events and recent population dynamics (e.g. population bottlenecks or several generations in captivity).     

Antipredatory Response and Food Intake in Wood Mice (Apodemus sylvaticus) under Simulated Predation Risk by Resident and Novel Carnivorous Predators

Chemical signals left by predators are a potential source of information about the risk of predation, and small mammals are known to take them into account when making decisions. We investigated whether wood mice (Apodemus sylvaticus) are more likely to avoid the faeces of resident predators (red fox Vulpes vulpes and common genet Genetta genetta) vs. a novel predator (European pine marten Martes martes). Odour recognition would increase perceived predation risk and reduce food intake by individual mice. Wood mice response to predators was analysed by live‐trapping using two untreated controls (baited/non‐baited) and traps experimentally manipulated with three predator treatments (faeces of red fox, common genet or pine marten). Traps were baited with 4 g of toasted corn, and food intake by wood mice was determined as the amount of bait remaining in each trap. We found that traps treated with faeces of resident predators were the most avoided, and the number of captures in traps treated with pine marten faeces was similar to the control‐baited traps. The variation found in food intake was explained by the interaction between the types of treatment and breeding condition. Food intake was similar in control‐baited traps and in traps with faeces of pine marten, but when predation risk by resident predators (red fox and common genet) was simulated, breeders reduced food intake significantly as compared to non‐breeders. These results indicate that predator recognition and feeding behaviour under predation risk depend on individual factors and the balance of costs‐benefits in each particular predation risk situation at a given place and time.     

Does a top predator reduce the predatory impact of an invasive mesopredator on an endangered rodent?

The mesopredator release hypothesis (MRH) predicts that reduced abundance of top‐order predators results in an increase in the abundance of smaller predators (mesopredators) due to a reduction in intra‐guild predation and competition. The irruption of mesopredators that follows the removal of top‐order predators can have detrimental impacts on the prey of the mesopredators. Here we investigated the mechanisms via which the presence of a top‐order predator can benefit prey species. We tested predictions made according to the MRH and foraging theory by contrasting the abundances of an invasive mesopredator (red fox Vulpes vulpes) and an endangered prey species (dusky hopping mouse Notomys fuscus), predator diets, and N. fuscus foraging behaviour in the presence and absence of a top‐predator (dingo Canis lupus dingo). As predicted by the MRH, foxes were more abundant where dingoes were absent. Dietary overlap between sympatric dingoes and foxes was extensive, and fox was recorded in 1 dingo scat possibly indicating intra‐guild predation. Notomys fuscus were more likely to occur in fox scats than dingo scats and as predicted by the MRH N. fuscus were less abundant in the absence of dingoes. The population increase of N. fuscus following rainfall was dampened in the absence of dingoes suggesting that mesopredator release can attenuate bottom‐up effects, although it remains conceivable that differences in grazing regimes associated with dingo exclusion could have also influenced N. fuscus abundance. Notomys fuscus exhibited lower giving‐up densities in the presence of dingoes, consistent with the prediction that their perceived risk of predation would be lower and foraging efficiency greater in the presence of a top‐predator. Our results suggest that mesopredator suppression by a top predator can create a safer environment for prey species where the frequency of fatal encounters between predators and prey is reduced and the non‐consumptive effects of predators are lower.     

Olfactory Predator Discrimination in Yellow‐Bellied Marmots

The mechanism underlying olfactory predator identification may be relatively experience‐independent, or it may rely on specific experience with predators. A mechanism by which prey might identify novel predators relies on the inevitable creation of sulfurous metabolites that are then excreted in the urine of carnivorous mammals. We tested whether free‐living, yellow‐bellied marmots (Marmota flaviventris) and mid‐sized herbivores that fall prey to a variety of carnivorous mammals could discriminate herbivore (elk—Cervus elephas) urine from predator (red fox—Vulpes vulpes, coyote—Canis latrans, mountain lion—Felis concolor, wolf—Canis lupus) urine, a novel herbivore (moose—Alces alces), and a distilled water control. We further asked how specific this assessment was by testing whether marmots responded differently to predators representing different levels of risk and to familiar vs. unfamiliar predators. We found that marmots responded more to urine from coyotes (a familiar predator on adults), mountain lions (a potentially unfamiliar predator that could kill adults) and wolves (a locally extinct predator that could kill adults) than to elk urine (a non‐predator). Red fox (a predator that poses a risk only to recently emerged marmot pups) urine elicited a less substantial (but not significantly so) response than coyote urine. Marmots can identify predators, even novel ones, using olfactory cues, suggesting that experience with a specific predator is not required to identify potential threats.     

An island-wide predator manipulation reveals immediate and long-lasting matching of risk by prey

Anti-predator behaviour affects prey population dynamics, mediates cascading effects in food webs and influences the likelihood of rapid extinctions. Predator manipulations in natural settings provide a rare opportunity to understand how prey anti-predator behaviour is affected by large-scale changes in predators. Here, we couple a long-term, island-wide manipulation of an important rodent predator, the island fox (Urocyon littoralis), with nearly 6 years of measurements on foraging by deer mice (Peromyscus maniculatus) to provide unequivocal evidence that prey closely match their foraging behaviour to the number of fox predators present on the island. Peromyscus maniculatus foraging among exposed and sheltered microhabitats (a measure of aversion to predation risk) closely tracked fox density, but the nature of this effect depended upon nightly environmental conditions known to affect rodent susceptibility to predators. These effects could not be explained by changes in density of deer mice over time. Our work reveals that prey in natural settings are cognizant of the dynamic nature of their predators over timescales that span many years, and that predator removals spanning many generations of prey do not result in a loss of anti-predator behaviour.     

Responses of naïve and experienced European rabbits to predator odour

The response of prey species to predator scent has been investigated in many mammalian species; however, there is little information about the responses of European wild rabbits at the population level. Therefore, we conducted a simple experiment to investigate the behavioural response of a rabbit population to native predator cues in the wild. We compared the response to the scent of a predator (red fox) in a wild rabbit population bred in semi-natural conditions and naïve to terrestrial predators with the response of a population in a similar environment where terrestrial predators were present. The response to predators was based on rabbit abundance, inferred from pellet counts and measured by the defecation rate per day (DRD). Our results indicate that rabbits responded to the odour of fox faeces in the treatment warrens, resulting in a lower DRD. The main anti-predator behaviour observed was spatial avoidance (warren abandonment), which seemed to be more accentuated for rabbits who had not previously had contact with foxes in the plot where terrestrial predators were excluded. In both the fenced and the unfenced plot, the differences in the effect of the predator odour between the control and treatment warrens disappeared after cessation of treatment, suggesting a flexible and adaptive behaviour of rabbits to predator cues.

     

Know thy enemy: Behavioural response of a native mammal (Rattus lutreolus velutinus) to predators of different coexistence histories

Abstract Predation is recognized as a major selective pressure influencing population dynamics and evolutionary processes. Prey species have developed a variety of predator avoidance strategies, not least of which is olfactory recognition. However, within Australia, European settlement has brought with it a number of introduced predators, perhaps most notably the red fox (Vulpes vulpes) and domestic cat (Felis catus), which native prey species may be unable to recognize and thus avoid due to a lack of coexistence history. This study examined the response of native Tasmanian swamp rats (Rattus lutreolus velutinus) to predators of different coexistence history (native predator‐ spotted‐tail quoll (Dasyurus maculatus), domestic cats and the recently introduced red fox). We used an aggregate behavioural response of R. l. velutinus to predator integumental odour in order to assess an overall behavioural response to predation risk. Rattus lutreolus velutinus recognized the integumental odour of the native quoll (compared with control odours) but did not respond to either cat or fox scent (compared with control odur). In contrast, analyses of singular behaviours resulted in the conclusion that rats did not respond differentially to either native or introduced predators, as other studies have concluded. Therefore, measuring risk assessment behaviours at the level of overall aggregate response may be more beneficial in understanding and analysing complex behavioural patterns such as predator detection and recognition. These results suggest that fox and cat introductions (and their interactive effects) may have detrimental impacts upon small native Tasmanian mammals due to lack of recognition and thus appropriate responses.     

Behavioural responses of free‐ranging western grey kangaroos (Macropus fuliginosus) to olfactory cues of historical and recently introduced predators

Predation risk influences foraging decisions and time allocation of prey species, and may result in habitat shifts from potentially dangerous to safer areas. We examined a wild population of western grey kangaroos (Macropus fuliginosus) to test the efficacy of predator faecal odour in influencing time allocated to different behaviours and inducing changes in habitat use. Kangaroos were exposed to fresh faeces of a historical predator, the dingo (Canis lupus dingo), a recently introduced predator, the red fox (Vulpes vulpes), a herbivore (horse, Equus caballus) and an unscented control simultaneously. Kangaroos did not increase vigilance in predator‐scented areas. However, they investigated odour sources by approaching and sniffing; more time was spent investigating fox odour than control odours. Kangaroos then exhibited a clear anti‐predator response to predator odours, modifying their space use by rapidly escaping, then avoiding fox and dingo odour sources. Our results demonstrate that wild western grey kangaroos show behavioural responses to predator faeces, investigating then avoiding these olfactory cues of potential predation risk, rather than increasing general vigilance. This study contributes to our understanding of the impact of introduced mammalian predators on marsupial prey and demonstrates that a native Australian marsupial can recognize and respond to the odour of potential predators, including one that has been recently introduced.     

Do Australian small mammals respond to native and introduced predator odours?

Abstract Coevolution is thought to have led to many small mammal species avoiding the scent marks of their main mammalian predators, as they provide a reliable cue to predation risk. Most support for this hypothesis comes from northern hemisphere predator/prey systems, however, it is unclear whether this avoidance of predator faecal odour occurs in Australia's mammalian fauna, which has evolved in relative isolation from the rest of the world, and is dominated by marsupials rather than placentals. We tested this theory for an Australian system with marsupial and placental predators and prey, that share a long‐term (>1 million years) or short‐term (<150 years) exposure to each other. The predators were the native marsupial tiger quoll Dasyurus maculatus and the introduced placental red fox Vulpes vulpes. The potential prey were three native rodent species, the bush rat Rattus fuscipes, the swamp rat Rattus lutreolus, the eastern chestnut mouse Pseudomys gracilicaudatus, and the marsupial brown antechinus Antechinus stuartii. Small mammals were captured in Elliott traps with 1/3 of traps treated with fox faeces, 1/3 treated with quoll faeces and the remainder left untreated. The native rodent species all showed avoidance of both tiger quoll and red fox odours whereas the marsupial antechinus showed no responses to either odour. Either predator odour avoidance has not evolved in this marsupial or their reaction to predator odours may be exhibited in ways which are not recognizable through trapping. The avoidance by the rodents of fox odour as well as quoll odour indicates this response may either be due to common components in fox and quoll odour, or it may be a recently evolved response.     

Predators,fire or resources: What drives the distribution of herbivores in fragmented mesic forests?

Trophic interactions and disturbance events can shape the structure and function of ecosystems. However, the effects of drivers such as predation, fire and climatic variables on species distributions are rarely considered concurrently. We used a replicated landscape‐scale predator management experiment to compare the effects of red fox Vulpes vulpes control, time‐since‐fire, vegetation type and other environmental variables on native herbivore distributions. Occurrence data for four native herbivores and an invasive predator – the red fox – were collected from 240 sites across three baited (for lethal fox control) and three unbaited forest blocks (4659–9750 ha) in south‐western Victoria, Australia, and used to build species distribution models. The herbivore taxa were as follows: red‐necked wallaby Macropus rufogriseus, black wallaby Wallabia bicolour, grey kangaroo Macropus fuligenosus and Macropus giganteus and common brushtail possum Trichosurus vulpecula. Fox control and fire had little effect on herbivore occurrence, despite the literature suggesting it can influence abundance, while climate, proximity to farmland and topography were more influential. This may be because the region’s high productivity and agricultural pastures subsidise food resources for both predators and prey within the forest blocks and so dampen trophic interactions. Alternatively, these drivers may affect herbivore abundance, but not herbivore occurrence. Understanding the drivers of herbivore distributions is an important step in predicting the effects of herbivory on other species, particularly after management interventions such as predator control and prescribed burns.     

Exploratory behaviour and novel predator recognition: behavioural correlations across contexts

It was hypothesized that the exploratory behaviour of an individual measured in a novel environment could predict its behaviour in response to a novel predator. This study examined novel predator recognition in the western mosquitofish Gambusia affinis, a species with individual differences in risk‐taking, activity and exploration in novel environments. Prey responded with characteristic shoaling and avoidance in response to native predators, but did not show characteristic antipredator behaviour towards novel predators. Furthermore, G. affinis exhibited individual‐level behavioural correlations across contexts but only when prey were tested with native predators. This could be the result of native predatory selection on behavioural correlations in the prey species.     

Red fox trap success is correlated with piping plover chick survival

Predation management is an important component of managing species of conservation concern. The piping plover (Charadrius melodus; plover), a disturbance-dependent and conservation-reliant shorebird that nests on sandy beaches and barrier islands on the Atlantic Coast, was listed under the United States Endangered Species Act in 1986, with habitat loss and predation stated as key causes of its decline. We evaluated the relationship between a suite of predators and plover chick survival from 2015–2018. We used a camera grid to establish indices of the abundance of 3 known chick predators: red fox (Vulpes vulpes), raccoon (Procyon lotor), and domestic cat. We used camera detections in a survival model to assess potential relationships between predator species detection and plover chick survival. Plover chick survival was negatively related with red fox detection, but not with detection of the other 2 predators. In addition to the correlation with red fox detections, chick survival was negatively related to high plover nesting density. Our results suggest that red foxes were predators of piping plover chicks during our study, likely augmented by other density-dependent sources of mortality. Targeted predator management could aid in conservation of piping plovers in this system as a short-term solution, but long-term recovery plans must also address habitat limitation.     

Effects of long‐term fox baiting on species composition and abundance in an Australian lizard community

Abstract We report on the effects of almost a decade of 1080‐fox baiting on a lizard community in a mosaic Australian habitat. Replicated comparisons of baited versus non‐baited control areas with near‐identical histories of bush fires, grazing and climate showed a higher density of red fox tracks (Canis vulpes) in the non‐baited areas. Furthermore, the fox‐baited areas showed a more than five times higher density of sand goannas (Varanus gouldii), a species that strongly overlaps the red fox in food niche breadth and is itself a direct target of fox predation, in particular its eggs and young. Exclusion of predators from a natural habitat led to significant increases in the density of small lizards, suggesting that predation can drive lizard population dynamics in this ecosystem. Replicated pitfall‐trapping in three habitats in the control areas (with high fox and low goanna density) versus the baited areas (with low fox and high goanna density) showed that fox baiting had positive effects on the density of diurnal scincid lizards in open grassland, whereas the control areas showed higher density of nocturnal gecko lizards. Our interpretation is that fox removal may result in a shift in the top predator towards the sand goanna. Historically, this indigenous, endemic species was the natural top predator. It has co‐evolved with its prey and that may have moulded it into a more efficient lizard predator per encounter than the introduced fox.     

Death feigning as an adaptive anti‐predator behaviour: Further evidence for its evolution from artificial selection and natural populations

Death feigning is considered to be an adaptive antipredator behaviour. Previous studies on Tribolium castaneum have shown that prey which death feign have a fitness advantage over those that do not when using a jumping spider as the predator. Whether these effects are repeatable across species or whether they can be seen in nature is, however, unknown. Therefore, the present study involved two experiments: (a) divergent artificial selection for the duration of death feigning using a related species T. freemani as prey and a predatory bug as predator, demonstrating that previous results are repeatable across both prey and predator species, and (b) comparison of the death‐feigning duration of T. castaneum populations collected from field sites with and without predatory bugs. In the first experiment, T. freemani adults from established selection regimes with longer durations of death feigning had higher survival rates and longer latency to being preyed on when they were placed with predatory bugs than the adults from regimes selected for shorter durations of death feigning. As a result, the adaptive significance of death‐feigning behaviour was demonstrated in another prey–predator system. In the second experiment, wild T. castaneum beetles from populations with predators feigned death longer than wild beetles from predator‐free populations. Combining the results from these two experiments with those from previous studies provided strong evidence that predators drive the evolution of longer death feigning.     

The fluctuating world of a tundra predator guild: bottom‐up constraints overrule top‐down species interactions in winter

Global warming is predicted to change ecosystem functioning and structure in Arctic ecosystems by strengthening top‐down species interactions, i.e. predation pressure on small herbivores and interference between predators. Yet, previous research is biased towards the summer season. Due to greater abiotic constraints, Arctic ecosystem characteristics might be more pronounced in winter. Here we test the hypothesis that top‐down species interactions prevail over bottom‐up effects in Scandinavian mountain tundra (Northern Sweden) where effects of climate warming have been observed and top‐down interactions are expected to strengthen. But we test this ‘a priori’ hypothesis in winter and throughout the 3–4 yr rodent cycle, which imposes additional pulsed resource constraints. We used snowtracking data recorded in 12 winters (2004–2015) to analyse the spatial patterns of a tundra predator guild (arctic fox Vulpes lagopus, red fox Vulpes vulpes, wolverine Gulo gulo) and small prey (ptarmigan, Lagopus spp). The a priori top‐down hypothesis was then tested through structural equation modelling, for each phase of the rodent cycle. There was weak support for this hypothesis, with top‐down effects only discerned on arctic fox (weakly, by wolverine) and ptarmigan (by arctic fox) at intermediate and high rodent availability respectively. Overall, bottom‐up constraints appeared more influential on the winter community structure. Cold specialist predators (arctic fox and wolverine) showed variable landscape associations, while the boreal predator (red fox) appeared strongly dependent on productive habitats and ptarmigan abundance. Thus, we suggest that the unpredictability of food resources determines the winter ecology of the cold specialist predators, while the boreal predator relies on resource‐rich habitats. The constraints imposed by winters and temporary resource lows should therefore counteract productivity‐driven ecosystem change and have a stabilising effect on community structure. Hence, the interplay between summer and winter conditions should determine the rate of Arctic ecosystem change in the context of global warming.     

Acoustic stimuli from predators trigger behavioural responses in aggregate caterpillars

Prey detect their predators through predator signals and cues and, consequently, respond with anti‐predatory behaviours to inhibit the action of their aggressors. Lepidopterans can intercept signals emitted by predators and may defend themselves through chemical, morphological or behavioural responses. In this study, we investigated the effect of acoustic stimuli of different predators on defensive behaviour of gregarious caterpillars. Our results demonstrated that Hylesia nigricans (Lepidoptera, Saturniidae) caterpillars alter their behaviour (i.e. abruptly raising the head) in response to the acoustic stimulus of the predators (i.e. predation risk signals from birds and wasps). The magnitude of this response depended on predator identity and caterpillar body size. Larger caterpillars responded more strongly to predatory stimuli than smaller caterpillars. However, regardless of the size of the caterpillars, they responded more strongly to the stimuli of wasps. In addition, we identified that H. nigricans caterpillars emit ultrasonic noise after detecting the stimuli of the predators – this noise seems to function as an alert about the risk of predation during the early stages of development (second and fifth instars). The duration of ultrasonic emission (i.e. milliseconds) increases with the number of repetitions of the stimuli (i.e. wing‐beat sounds of the wasps and insectivorous birds). These results provide novel information about predation risk in interactions among caterpillars and their predators, and indicate possible communication among invertebrates mediated by the risk of predation.     

Overcoming prey naiveté: Free‐living marsupials develop recognition and effective behavioral responses to alien predators in Australia

Naiveté in prey arises from novel ecological mismatches in cue recognition systems and antipredator responses following the arrival of alien predators. The multilevel naiveté framework suggests that animals can progress through levels of naiveté toward predator awareness. Alternatively, native prey may be preadapted to recognize novel predators via common constituents in predator odors or familiar predator archetypes. We tested predictions of these competing hypotheses on the mechanisms driving behavioral responses of native species to alien predators by measuring responses of native free‐living northern brown bandicoots (Isoodon macrourus) to alien red fox (Vulpes vulpes) odor. We compared multiple bandicoot populations either sympatric or allopatric with foxes. Bandicoots sympatric with foxes showed recognition and appropriate antipredator behavior toward fox odor via avoidance. On the few occasions bandicoots did visit, their vigilance significantly increased, and their foraging decreased. In contrast, bandicoots allopatric with foxes showed no recognition of this predator cue. Our results suggest that vulnerable Australian mammals were likely naïve to foxes when they first arrived, which explains why so many native mammals declined soon after fox arrival. Our results also suggest such naiveté can be overcome within a relatively short time frame, driven by experience with predators, thus supporting the multilevel naiveté framework.     

Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation

In many amphibian larvae a suite of morphological and behavioural characters varies together in an induced defence against predators, but it remains unclear which features are functionally related to defence. We independently manipulated behaviour and morphology in tadpoles of Hyla versicolor and assessed their consequences for swimming performance and predator escape. Data on burst swimming showed that tadpoles which accelerated rapidly were elongate, with shallow bodies and tails. Predator escape was measured by exposing tadpoles to predators (larval Anax dragonflies or larval Ambystoma salamanders) and recording time until death. Tadpoles were first reared for 30 days in ponds containing either caged Anax or no predators; individuals responded to predators by developing large brightly coloured tails and short bodies. We placed tadpoles of both morphological phenotypes into plastic tubs, and manipulated their behaviour using food and chemical cues from predators. Mortality risk experienced by the predator‐induced phenotype was about half that of the no‐predator phenotype, and risk increased with time spent swimming. An interaction between morphology and behaviour arose because increasing activity caused higher risk for tadpoles with deep tail fins but not shallow tail fins.     

Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

Functional and numerical responses of four lemming predators in high arctic Greenland

The high‐arctic tundra ecosystem has the world's simplest vertebrate predator–prey community, with only four predators preying upon one rodent species, the collared lemming (Dicrostonyx groenlandicus). We document the functional and numerical responses of all the four predators in NE Greenland. Using these data, we assess the impact of predation on the dynamics of the collared lemming with a 4 yr cycle and >100‐fold difference between maximum and minimum densities. All predator species feed mostly (>90%) on lemmings when lemming density is >1 ha^?1, but the shapes of the predators’ responses vary greatly. The snowy owl (Nyctea scandiaca) is present and breeds only when lemming densities at snowmelt are >2 ha^?1, giving rise to a step‐like numerical response. The long‐tailed skua (Stercorarius longicaudus) has a type III functional response and shifts from alternate food (mainly berries and insects) to lemmings with increasing lemming density. The skua surpasses all the other predators in summer by its total response. The type III functional response of the Arctic fox (Alopex lagopus) starts to increase at much lower lemming densities than the responses of the avian predators, but it has only a weak numerical response. Finally, the stoat (Mustela erminea) is the most specialized predator and the only one with a clearly delayed numerical response. According to their specific functional and numerical responses, each predator plays a key role at some point of the lemming cycle, but only the stoat has the potential to drive the lemming cycle. Stoat predation is greatly reduced in the winter preceding the lemming peak, and it reaches a maximum in the winter preceding the lowest lemming summer density. Stoat predation appears to maintain low lemming densities for at least two successive years. Our study provides empirical support for the specialist predator hypothesis about small mammal population cycles.