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When death comes: linking predator-prey activity patterns to timing of mortality to understand predation risk

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The assumption that activity and foraging are risky for prey underlies many predator-prey theories and has led to the use of predator-prey activity overlap as a proxy of predation risk. However, the simultaneous measures of prey and predator activity along with timing of predation required to test this assumption have not been available. Here, we used accelerometry data on snowshoe hares (Lepus americanus) and Canada lynx (Lynx canadensis) to determine activity patterns of prey and predators and match these to precise timing of predation. Surprisingly we found that lynx kills of hares were as likely to occur during the day when hares were inactive as at night when hares were active. We also found that activity rates of hares were not related to the chance of predation at daily and weekly scales, whereas lynx activity rates positively affected the diel pattern of lynx predation on hares and their weekly kill rates of hares. Our findings suggest that predator-prey diel activity overlap may not always be a good proxy of predation risk, and highlight a need for examining the link between predation and spatio-temporal behaviour of predator and prey to improve our understanding of how predator-prey behavioural interactions drive predation risk.
Cite this article: Shiratsuru S et al. 2023
When death comes: linking predatorprey
activity patterns to timing of mortality to
understand predation risk. Proc. R. Soc. B 290:
Received: 21 March 2023
Accepted: 21 April 2023
Subject Category:
Subject Areas:
behaviour, ecology, ecosystems
predatorprey, diel activity, time of predation,
predation risk, Lepus americanus,Lynx
Author for correspondence:
Shotaro Shiratsuru
These authors contributed equally.
Electronic supplementary material is available
online at
When death comes: linking predatorprey
activity patterns to timing of mortality to
understand predation risk
Shotaro Shiratsuru
, Emily K. Studd
, Stan Boutin
, Michael J. L. Peers
Yasmine N. Majchrzak
, Allyson K. Menzies
, Rachael Derbyshire
Thomas S. Jung
, Charles J. Krebs
, Rudy Boonstra
and Dennis L. Murray
Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2R3
Department of Biological Sciences, Thompson Rivers University, Kamloops, British Columbia, Canada V2C 0B8
Department of Natural Resource Sciences, McGill University, St-Anne-de-Bellevue, Québec, Canada H9X 3V9
Department of Biology, Trent University, Peterborough, Ontario, Canada
Department of Environment, Government of Yukon, Whitehorse, Yukon, Canada
Department of Renewable Resources, University of Alberta, Edmonton, Alberta, Canada
Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada
Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada
SS, 0000-0001-8747-9664; MJLP, 0000-0002-3014-2056; RB, 0000-0003-1959-1077
The assumption that activity and foraging are risky for prey underlies many
predatorprey theories and has led to the use of predatorprey activity over-
lap as a proxy of predation risk. However, the simultaneous measures of prey
and predator activity along with timing of predation required to test this
assumption have not been available. Here, we used accelerometry data on
snowshoe hares (Lepus americanus) and Canada lynx (Lynx canadensis)to
determine activity patterns of prey and predators and match these to precise
timing of predation. Surprisingly we found that lynx kills of hares were as
likely to occur during the day when hares were inactive as at night when
hares were active. We also found that activity rates of hares were not related
to the chance of predation at daily and weekly scales, whereas lynx activity
rates positively affected the diel pattern of lynx predation on hares and
their weekly kill rates of hares. Our findings suggest that predatorprey diel
activity overlap may not always be a good proxy of predation risk, and high-
light a need for examining the link between predation and spatio-temporal
behaviour of predator and prey to improve our understanding of how
predatorprey behavioural interactions drive predation risk.
1. Introduction
The fact that predators can only kill prey when they overlap in space and time [1]
has led to the belief that increased spatial [2,3] and temporal [4,5] overlap
between predators and prey correlates with predation risk. For example, diel
activity overlap between predator and prey is now increasingly used as a
proxy of predation risk [68]. However, although this may be a reasonable start-
ing assessment of perceived predation risk (e.g. high predator density or places
and times where and when predators are more likely to be present and active),
such overlap may not always be a good proxy of actual predation risk (the prob-
ability of predation). Assessment of predation risk in relation to behavioural
predatorprey interactions requires simultaneous measures of the behaviour of
predator and prey and predation rate, but such studies are still scarce (but see [9]).
Effects of predatorprey spatio-temporal overlap on predation can be
confounded by various environmental factors. For example, habitat character-
istics are potentially more important determinants of predation than
predatorprey spatial overlap [10], or diel patterns of predation can be modified
by anthropogenic disturbance while prey fail to adjust their temporal activity
pattern in response to it [11]. It is well documented that prey show a wide
© 2023 The Author(s) Published by the Royal Society. All rights reserved.
Full-text available
1 Movement is a key component of an animal's life history. While there are numerous factors that influence movement, there is an inherent link between a species' social ecology and its movement ecology. Despite this inherent relationship, the socio-spatial ecology of many species remains unknown, hampering ecological theory and conservation alike. Here, we use fine-scale GPS location data and continuous-time stochastic processes to study the socio-spatial ecology of 23 giant anteaters (Myrmecophaga tridactyla) in the Brazilian Cerrado. We found that individuals occupied stable home ranges with a mean area of 5.45 km 2 with males having significantly larger home ranges than females. The average amount of home-range overlap was low (0.20, n = 121 dyads), with no evidence that giant anteater home ranges were structured based on territorial, mate guarding, nor other social behaviour. We also identified a total of 2774 encounter events. Interestingly, both female-male and male-male dyads had significantly more encounters than female-female dyads, with two pronounced seasonal peaks in female-male encounters. Though encounters occurred frequently, associations between dyads were generally weak and there was little evidence of any correlated movement (mean amount of total correlation = 0.01). Collectively, these findings suggest giant anteaters are a solitary and largely asocial species that readily share space with conspecifics. Despite their present capacity to share space, the combined pressures of being condensed into smaller areas and decreased food availability due to increased pesticide use may see behavioural changes radiating throughout the population. Our study provides insight into heretofore unknown aspects of the socio-spatial ecology of this iconic, but understudied species, as well as crucial information for proactive area-based management. Ultimately, these findings contribute towards sustainable development while potentially maintaining the ecological integrity of giant anteaters and their habitats.
Full-text available
An animal’s daily use of time (their “diel activity”) reflects their adaptations, requirements, and interactions, yet we know little about the underlying processes governing diel activity within and among communities. Here we examine whether community-level activity patterns differ among biogeographic regions, and explore the roles of top-down versus bottom-up processes and thermoregulatory constraints. Using data from systematic camera-trap networks in 16 protected forests across the tropics, we examine the relationships of mammals’ diel activity to body mass and trophic guild. Also, we assess the activity relationships within and among guilds. Apart from Neotropical insectivores, guilds exhibited consistent cross-regional activity in relation to body mass. Results indicate that thermoregulation constrains herbivore and insectivore activity (e.g., larger Afrotropical herbivores are ~7 times more likely to be nocturnal than smaller herbivores), while bottom-up processes constrain the activity of carnivores in relation to herbivores, and top-down processes constrain the activity of small omnivores and insectivores in relation to large carnivores’ activity. Overall, diel activity of tropical mammal communities appears shaped by similar processes and constraints among regions reflecting body mass and trophic guilds.
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Wind speed can have multifaceted effects on organisms including altering thermoregulation, locomotion, and sensory reception. While forest cover can substantially reduce wind speed at ground level, it is not known if animals living in forests show any behavioural responses to changes in wind speed. Here, we explored how three boreal forest mammals, a predator and two prey, altered their behaviour in response to average daily wind speeds during winter. We collected accelerometer data to determine wind speed effects on activity patterns and kill rates of free-ranging red squirrels (n = 144), snowshoe hares (n = 101), and Canada lynx (n = 27) in Kluane, Yukon from 2015 to 2018. All 3 species responded to increasing wind speeds by changing the time they were active, but effects were strongest in hares, which reduced daily activity by 25%, and lynx, which increased daily activity by 25%. Lynx also increased the number of feeding events by 40% on windy days. These results highlight that wind speed is an important abiotic variable that can affect behaviour, even in forested environments.
Full-text available
Snowshoe hare cycles are one of the most prominent phenomena in ecology. Experimental studies point to predation as the dominant driving factor, but previous experiments combining food supplementation and predator removal produced unexplained multiplicative effects on density. We examined the potential interactive effects of food limitation and predation in causing hare cycles using an individual-based food-supplementation experiment over-winter across three cycle phases that naturally varied in predation risk. Supplementation doubled over-winter survival with the largest effects occurring in the late increase phase. Although the proximate cause of mortality was predation, supplemented hares significantly decreased foraging time and selected for conifer habitat, potentially reducing their predation risk. Supplemented hares also lost less body mass which resulted in the production of larger leverets. Our results establish a mechanistic link between how foraging time, mass loss and predation risk affect survival and reproduction, potentially driving demographic changes associated with hare cycles.
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The energetic consequences of body size, behaviour, and fine-scale environmental variation remain understudied, particularly among free-ranging carnivores, due to logistical and methodological challenges of studying them in the field. Here, we present novel activity, heart rate, and metabolic data on free-ranging Canada lynx (Lynx canadensis Kerr, 1792) to a) investigate intraspecific patterns of energy expenditure, particularly how they relate to body size, environmental conditions, and activity variation, and b) position lynx - a cold-climate, mesocarnivore - within interspecific allometries of carnivore energetics. Lynx demonstrated limited behavioural and metabolic responses to environmental conditions, despite extreme cold and moderate snow depths during our study, but marked body size patterns with larger lynx having higher activity and lower resting heart rate than smaller lynx. Compared to similar-sized carnivores, lynx were less active and had lower heart rate, likely due to their ambush hunting style, but higher energy expenditure, likely due to their cold-climate existence and access to abundant prey. Overall, lynx were more similar to other ambush hunters than to sympatric cold-climate species and mesocarnivores. Our data provide insight into the relative importance of abiotic and biotic drivers of carnivore energetics and the ways in which predators maintain energy balance in variable environments.
Full-text available
The activity level is a fundamental metric of animal behavior, related to the avoidance of predators, food acquisition, and thermoregulation. Animals need to weigh their activity budget to fulfill their energetic, social and reproductive requirements over the energetic costs of these activities. This task becomes further challenging for prey species, which also need to account for predation risk. To investigate the factors shaping proactive behavioral decisions leading prey species engagement in their diel activities, we implemented a multisite year-round monitoring study on the Iberian rabbit (Oryctolagus cuniculus algirus), a key prey species in Mediterranean ecosystems. We deployed remotely triggered cameras over 15 sites to continuously monitor Iberian rabbits' activity. We estimated activity levels from time-of-detection data from camera traps, and modeled it as a function of climatic, intraspecific, predation, and resource-related covariates. We found that Iberian rabbits exhibit a bimodal activity pattern peaking at sunrise and sunset, with a more pronounced peak occurring at sunrise during the nonbreeding season, and spend 9.15 ± 3.00 h/day (mean ± sd) active. Diel activity levels were negatively affected by extreme environmental temperatures and density dependence, demonstrating the privileged importance of social interactions and normothermia maintenance. We found mammalian predator activity and abundance to have near-negligible effects on the activity levels of this key prey, suggesting decreased antipredator behavior when risk is perceived as prolonged. Moreover, we argue that perceived risk may be more important than realized risk in shaping Iberian rabbits' activity level. These results provide valuable insights toward a comprehensive understanding of the factors underlying behavioral decisions made by prey species, relevant for maintaining their energetic and homeostatic balance.
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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.
Animals are facing novel ‘timescapes’ in which the stimuli entraining their daily activity patterns no longer match historical conditions due to anthropogenic disturbance. However, the ecological effects (e.g., altered physiology, species interactions) of novel activity timing are virtually unknown. We reviewed 1328 studies and found relatively few focusing on anthropogenic effects on activity timing. We suggest three hypotheses to stimulate future research: (i) activity-timing mismatches determine ecological effects, (ii) duration and timing of timescape modification influence effects, and (iii) consequences of altered activity timing vary biogeographically due to broad-scale variation in factors compressing timescapes. The continued growth of sampling technologies promises to facilitate the study of the consequences of altered activity timing, with emerging applications for biodiversity conservation.
Predation risk, the probability that a prey animal will be killed by a predator, is fundamental to theoretical and applied ecology. Predation risk varies with animal behavior and environmental conditions, yet attempts to understand predation risk in natural systems often ignore important ecological and environmental complexities, relying instead on proxies for actual risk such as predator–prey spatial overlap. Here we detail the ecological and environmental complexities driving disconnects between three stages of the predation sequence that are often assumed to be tightly linked: spatial overlap, encounters and prey capture. Our review highlights several major sources of variability in natural predator–prey systems that lead to the decoupling of spatial overlap estimates from actual encounter rates (e.g. temporal activity patterns, predator and prey movement capacity, resource limitations) and that affect the probability of prey capture given encounter (e.g. predator hunger levels, temporal, topographic and other environmental influences on capture success). Emerging technologies and statistical methods are facilitating a transition to a more spatiotemporally detailed, mechanistic understanding of predator–prey interactions, allowing for the concurrent examination of multiple stages of the predation sequence in mobile, free‐ranging animals. We describe crucial applications of this new understanding to fundamental and applied ecology, highlighting opportunities to better integrate ecological contingencies into dynamic predator–prey models and to harness a mechanistic understanding of predator–prey interactions to improve targeting and effectiveness of conservation interventions.
Food availability and temporal variation in predation risk are both important determinants of the magnitude of antipredator responses, but their effects have rarely been examined simultaneously, particularly in wild prey. Here, we determine how food availability and long‐term predation risk affect antipredator responses to acute predation risk by monitoring the foraging response of free‐ranging snowshoe hares (Lepus americanus) to an encounter with a Canada lynx (Lynx canadensis) in Yukon, Canada, over 4 winters (from 2015‐2016 to 2018‐2019). We examined how this response was influenced by natural variation in long‐term predation risk (two‐month mortality rate of hares) while providing some individuals with supplemental food. On average, snowshoe hares reduced foraging time up to 10 hours after coming into close proximity (≤ 75 m) with lynx, and reduced foraging time an average of 15.28 ± 7.08 minutes per lynx encounter. Hares tended to respond more strongly when the distance to lynx was shorter. More importantly, the magnitude of hares’ antipredator response to a lynx encounter was affected by the interaction between food‐supplementation and long‐term predation risk. Food‐supplemented hares reduced foraging time more than control hares after a lynx encounter under low long‐term risk, but decreased the magnitude of the response as long‐term risk increased. In contrast, control hares increased the magnitude of their response as long‐term risk increased. Our findings show that food availability and long‐term predation risk interactively drive the magnitude of reactive antipredator response to acute predation risk. Determining the factors driving the magnitude of antipredator responses would contribute to a better understanding of the indirect effects of predators on prey populations.
Perceived predation risk and the resulting antipredator behaviour varies across space, time and predator identity. Communities with multiple predators that interact and differ in their use of space, time of activity and hunting mode create a complex landscape for prey to avoid predation. Anthropogenic presence and disturbance have the potential to shift interactions among predators and prey and the where and when encounters occur. We examined how white‐tailed deer Odocoileus virginianus fawn spatiotemporal antipredator behaviour differed along an anthropogenic disturbance gradient that had black bears Ursus americanus , coyotes Canis latrans , bobcats Lynx rufus and humans present. We quantified (a) spatial co‐occurrence in species distributions, (b) temporal overlap across the diel cycle and (c) spatiotemporal associations between humans, bears, coyotes, bobcats, adult male deer and fawns. We also examined how deer vigilance behaviour changed across the anthropogenic disturbance gradient and survey duration. Anthropogenic disturbance influenced spatiotemporal co‐occurrence across multiple scales, often increasing spatiotemporal overlap among species. In general, species’ spatial co‐occurrence was neutral or positive in anthropogenically disturbed environments. Bears and fawns, coyotes and adult male deer, and bobcats and fawns all had higher temporal overlap in the agriculture‐development matrix sites. In addition, factors that influenced deer vigilance (e.g. distance to forest edge and predator relative abundance) in the agriculture‐development matrix sites did not in the forest matrix site. By taking into account the different antipredator behaviours that can be detected and the different scales these behaviours might occur, we were able to gain a more comprehensive picture of how humans reduce available niche space for wildlife, creating the neutral and positive spatiotemporal associations between species that studies have been seeing in more disturbed areas.