Predator home range size mediates indirect interactions between prey species in an arctic vertebrate community.

Indirect interactions are widespread among prey species that share a common predator, but the underlying mechanisms driving these interactions are often unclear, and our ability to predict their outcome is limited. Changes in behavioural traits that impact predator space use could be a key proximal mechanism mediating indirect interactions, but there is little empirical evidence of the causes and consequences of such behavioural-numerical response in multispecies systems. Here, we investigate the complex ecological relationships between seven prey species sharing a common predator. We used a path analysis approach on a comprehensive 9-year data set simultaneously tracking predator space use, prey densities and prey mortality rate on key species of a simplified Arctic food web. We show that high availability of a clumped and spatially predictable prey (goose eggs) leads to a twofold reduction in predator (arctic fox) home range size, which increases local predator density and strongly decreases nest survival of an incidental prey (American golden plover). On the contrary, a scattered cyclic prey with potentially lower spatial predictability (lemming) had a weaker effect on fox space use and an overall positive impact on the survival of incidental prey. These contrasting effects underline the importance of studying behavioural responses of predators in multiprey systems and to explicitly integrate behavioural-numerical responses in multispecies predator-prey models.

Predator-mediated interactions through changes in predator home range size can lead to local prey exclusion.

The strength of indirect biotic interactions is difficult to quantify in the wild and can alter community composition. To investigate whether the presence of a prey species affects the population growth rate of another prey species, we quantified predator-mediated interaction strength using a multi-prey mechanistic model of predation and a population matrix model. Models were parametrized using behavioural, demographic and experimental data from a vertebrate community that includes the arctic fox (Vulpes lagopus), a predator feeding on lemmings and eggs of various species such as sandpipers and geese. We show that the positive effects of the goose colony on sandpiper nesting success (due to reduction of search time for sandpiper nests) were outweighed by the negative effect of an increase in fox density. The fox numerical response was driven by changes in home range size. As a result, the net interaction from the presence of geese was negative and could lead to local exclusion of sandpipers. Our study provides a rare empirically based model that integrates mechanistic multi-species functional responses and behavioural processes underlying the predator numerical response. This is an important step forward in our ability to quantify the consequences of predation for community structure and dynamics.

A mechanistic model of functional response provides new insights into indirect interactions among arctic tundra prey.

Prey handling processes are considered a dominant mechanism leading to short-term positive indirect effects between prey that share a predator. However, a growing body of research indicates that predators are not necessarily limited by such processes in the wild. Density-dependent changes in predator foraging behavior can also generate positive indirect effects but they are rarely included as explicit functions of prey densities in functional response models. With the aim of untangling proximate mechanisms of species interactions in natural communities and improving our ability to quantify interaction strength, we extended the multi-prey version of the Holling disk equation by including density-dependent changes in predator foraging behavior. Our model, based on species traits and behavior, was inspired by the vertebrate community of the arctic tundra, where the main predator (the arctic fox) is an active forager feeding primarily on cyclic small rodent (lemming) and eggs of various tundra-nesting bird species. Short-term positive indirect effects of lemmings on birds have been documented over the circumpolar Arctic but the underlying mechanisms remain poorly understood. We used a unique data set, containing high-frequency GPS tracking, accelerometer, behavioral, and experimental data to parameterize the multi-prey model, and a 15-year time series of prey densities and bird nesting success to evaluate interaction strength between species. We found that (1) prey handling processes play a minor role in our system and (2) changes in arctic fox daily activity budget and distance traveled can partly explain the predation release on birds observed during lemming peaks. These adjustments in predator foraging behavior with respect to the main prey density thus appear as the dominant mechanism leading to positive indirect effects commonly reported among arctic tundra prey. Density-dependent changes in functional response components have been little studied in natural vertebrate communities and deserve more attention to improve our ability to quantify the strength of species interactions.

Digging into the behaviour of an active hunting predator: arctic fox prey caching events revealed by accelerometry.

BACKGROUND: Biologging now allows detailed recording of animal movement, thus informing behavioural ecology in ways unthinkable just a few years ago. In particular, combining GPS and accelerometry allows spatially explicit tracking of various behaviours, including predation events in large terrestrial mammalian predators. Specifically, identification of location clusters resulting from prey handling allows efficient location of killing events. For small predators with short prey handling times, however, identifying predation events through technology remains unresolved. We propose that a promising avenue emerges when specific foraging behaviours generate diagnostic acceleration patterns. One such example is the caching behaviour of the arctic fox (Vulpes lagopus), an active hunting predator strongly relying on food storage when living in proximity to bird colonies. METHODS: We equipped 16 Arctic foxes from Bylot Island (Nunavut, Canada) with GPS and accelerometers, yielding 23 fox-summers of movement data. Accelerometers recorded tri-axial acceleration at 50 Hz while we obtained a sample of simultaneous video recordings of fox behaviour. Multiple supervised machine learning algorithms were tested to classify accelerometry data into 4 behaviours: motionless, running, walking and digging, the latter being associated with food caching. Finally, we assessed the spatio-temporal concordance of fox digging and greater snow goose (Anser caerulescens antlanticus) nesting, to test the ecological relevance of our behavioural classification in a well-known study system dominated by top-down trophic interactions. RESULTS: The random forest model yielded the best behavioural classification, with accuracies for each behaviour over 96%. Overall, arctic foxes spent 49% of the time motionless, 34% running, 9% walking, and 8% digging. The probability of digging increased with goose nest density and this result held during both goose egg incubation and brooding periods. CONCLUSIONS: Accelerometry combined with GPS allowed us to track across space and time a critical foraging behaviour from a small active hunting predator, informing on spatio-temporal distribution of predation risk in an Arctic vertebrate community. Our study opens new possibilities for assessing the foraging behaviour of terrestrial predators, a key step to disentangle the subtle mechanisms structuring many predator-prey interactions and trophic networks.

Extensive daily movement rates measured in territorial arctic foxes.

An animal's movement rate is a central metric of movement ecology as it correlates with its energy acquisition and expenditure. Obtaining accurate estimates of movement rate is challenging, especially in small highly mobile species where GPS battery size limits fix frequency, and geolocation technology limits positions' precision. In this study, we used high GPS fix frequencies to evaluate movement rates in eight territorial arctic foxes on Bylot Island (Nunavut, Canada) in July-August 2018. We also assessed the effects of fix interval and location error on estimated movement rates. We obtained 96 fox-days of data with a fix interval of 4 min and 12 fox-days with an interval of 30 s. We subsampled the latter dataset to simulate six longer fix intervals ranging from 1 to 60 min and estimated daily distances traveled by adding linear distances between successive locations. When estimated with a fix interval of 4 min, daily distances traveled by arctic foxes averaged 51.9 ± 11.7 km and reached 76.5 km. GPS location error averaged 11 m. Daily distances estimated at fix intervals longer than 4 min were greatly underestimated as fix intervals increased, because of linear estimation of tortuous movements. Conversely, daily distances estimated at fix intervals as small as 30 s were likely overestimated due to location error. To our knowledge, no other territorial terrestrial carnivore was shown to routinely travel daily distances as large as those observed here for arctic foxes. Our results generate new hypotheses and research directions regarding the foraging ecology of highly mobile predators. Furthermore, our empirical assessment of the effects of fix interval and location error on estimated movement rates can guide the design and interpretation of future studies on the movement ecology of small opportunistic foragers.

Prey and habitat distribution are not enough to explain predator habitat selection: addressing intraspecific interactions, behavioural state and time.

BACKGROUND: Movements and habitat selection of predators shape ecological communities by determining the spatiotemporal distribution of predation risk. Although intraspecific interactions associated to territoriality and parental care are involved in predator habitat selection, few studies have addressed their effects simultaneously with those of prey and habitat distribution. Moreover, individuals require behavioural and temporal flexibility in their movement decisions to meet various motivations in a heterogeneous environment. To untangle the relative importance of ecological determinants of predator fine-scale habitat selection, we studied simultaneously several spatial, temporal, and behavioural predictors of habitat selection in territorial arctic foxes (Vulpes lagopus) living within a Greater snow goose (Anser caerulescens atlantica) colony during the reproductive season. METHODS: Using GPS locations collected at 4-min intervals and behavioural state classification (active and resting), we quantified how foxes modulate state-specific habitat selection in response to territory edges, den proximity, prey distribution, and habitats. We also assessed whether foxes varied their habitat selection in response to an important phenological transition marked by decreasing prey availability (goose egg hatching) and decreasing den dependency (emancipation of cubs). RESULTS: Multiple factors simultaneously played a key role in driving habitat selection, and their relative strength differed with respect to the behavioural state and study period. Foxes avoided territory edges, and reproductive individuals selected den proximity before the phenological transition. Higher goose nest density was selected when foxes were active but avoided when resting, and was less selected after egg hatching. Selection for tundra habitats also varied through the summer, but effects were not consistent. CONCLUSIONS: We conclude that constraints imposed by intraspecific interactions can play, relative to prey distribution and habitat characteristics, an important role in the habitat selection of a keystone predator. Our results highlight the benefits of considering behavioural state and seasonal phenology when assessing the flexibility of predator habitat selection. Our findings indicate that considering intraspecific interactions is essential to understand predator space use, and suggest that using predator habitat selection to advance community ecology requires an explicit assessment of the social context in which movements occur.