Volume 152, Part A, 1 December 2015, Pages 244–248
- a Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, NO-1432 Ås, Norway
- b Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden
- c Grimsö Wildlife Research Station, Department of Ecology, Swedish University of Agricultural Sciences, SE–730 91 Riddarhyttan, Sweden
- d Department of Forestry and Wildlife Management, Hedmark University College, Campus Evenstad, NO-2418 Elverum, Norway
- e Medtronic Inc., Mounds View, MN 55112, USA
- f Department of Surgery, University of Minnesota, Minneapolis, MN 55455, USA
- g Örebro University, Faculty of Health, Department of Cardiology, SE-701 82 Örebro, Sweden
- h Norwegian Institute for Nature Research, NO-7485 Trondheim, Norway
- Received 3 July 2015, Revised 22 September 2015, Accepted 29 September 2015, Available online 22 October 2015
- Under a Creative Commons license
Open Access
Highlights
- •
- Heart rate variability can be considered as an indicator of stress.
- •
- Lower heart rate variability indicated stress in brown bears when close to humans.
- •
- Autumn, when humans were more in the forest, was the season with highest stress.
- •
- Our findings provide evidence of a human-induced landscape of fear in brown bears.
Abstract
Human
persecution is a major cause of mortality for large carnivores.
Consequently, large carnivores avoid humans, but may use human-dominated
landscapes by being nocturnal and elusive. Behavioral studies indicate
that certain ecological systems are “landscapes of fear”, driven by
antipredator behavior. Because behavior and physiology are closely
interrelated, physiological assessments may provide insight into the
behavioral response of large carnivores to human activity. To elucidate
changes in brown bears' (Ursus arctos) behavior associated with
human activity, we evaluated stress as changes in heart rate (HR) and
heart rate variability (HRV) in 12 GPS-collared, free-ranging bears, 7
males and 5 females, 3–11 years old, using cardiac-monitoring devices.
We applied generalized linear regression models with HR and HRV as
response variables and chest activity, time of day, season, distance
traveled, and distance to human settlements from GPS positions recorded
every 30 min as potential explanatory variables. Bears exhibited lower
HRV, an indication of stress, when they were close to human settlements
and especially during the berry season, when humans were more often in
the forest, picking berries and hunting. Our findings provide evidence
of a human-induced landscape of fear in this hunted population of brown
bears.
Keywords
- Brown bear;
- Ursus arctos;
- Heart rate;
- Heart rate variability;
- Human disturbance;
- Wildlife
1. Introduction
Humans
and human activity are the largest threat for large carnivores
worldwide, because of habitat loss and degradation, prey depletion and
human harvest, and several species are threatened by extinction [43]. Large carnivores come into conflict with people because they prey on livestock or pets [20] and [53], compete with hunters for wild game [33], and because they can harm people and are perceived as dangerous [44]. Human persecution, often due to these conflicts, is the main mortality cause in large carnivores [57].
Consequently,
large carnivores avoid humans and human activity, but some species can
utilize human-dominated landscapes by altering their prey base, range
use, behavior, and/or becoming more nocturnal and elusive [4], [21] and [38].
Nevertheless, human population growth and urbanization continue to
bring people into the areas where large carnivore populations persist [42] and [54], thus the future survival of these species depends partly on their ability to adapt to human-dominated landscapes [26] and [58].
Behavioral
studies of predators and prey have led to viewing ecological systems
conceptually as “landscapes of fear”, driven by trait-mediated,
behavioral effects of predators [8].
The argument is that predation causes mortality, but both predation
risk and disturbance affect population dynamics by forcing individuals
to invest in antipredator behavior (e.g., vigilance) and thus discard
more profitable activities (e.g., foraging and resting; [16]). This behavioral trade-off has gained increased recognition as a means of understanding predator–prey interactions (e.g., [39]) and, ultimately, the processes that determine the structure and stability of ecological systems [45].
In this context, predator–prey and predator-avoidance theory may
provide insight into the effects human activity have on wildlife [16]. Thus, large carnivores can be viewed as prey avoiding predation by humans in a “landscape of fear” [34].
The brown bear (Ursus arctos)
is a large carnivore that often inhabits multiuse human-dominated
landscapes, where they avoid humans both spatially and temporally. At
the landscape scale in northern Europe, adult bears prefer to live in
rugged terrain far from human settlements [28], [31] and [48]
and at a finer scale they select daytime resting sites with more
vegetation cover when closer to human settlements and when more people
are in the forest [34]. Temporally, the bears avoid humans by being active at night, and inactive and resting in cover during the day [29],
but adjust their circadian behavior to be more nocturnal in populated
areas than in remote areas and in seasons with more human activity, e.g.
during the annual bear hunting season [35].
Bears also respond to direct encounters with humans by becoming less
active during daytime hours for the next several days, which may also
alter their optimum allocation of time for resting and foraging [36].
Behavior
and physiology are closely interconnected. Physiological assessments
can thus be useful in explaining cause-and-effect relationships, e.g.,
in understanding the influence of anthropogenic disturbance on an
organism's condition and health [9].
Heart rate (HR) and heart rate variability (HRV) have been used in both
humans and mammals to measure both physiological and psychological
stress [18], [27] and [59].
Heart rate is typically calculated from the R-R interval (time between
heart beats) and heart rate variability as the variability in the R-R
interval [40].
Heart rate variability can be viewed as the dynamic interaction between
the acceleratory sympathetic and the deceleratory parasympathetic
nervous systems' input to the heart. A low HRV indicates increased
sympathetic/decreased parasympathetic tone (less variability, “fight or
flight” responses) and a high HRV indicates increased
parasympathetic/decreased sympathetic tone (more variability, “rest and
digest” responses) [47]. Although HR is highly affected by movement, HRV is less so. Stress affects the concentration of several hormones [5] and also produces changes in HRV [11] and [51], thus HRV can be considered an indicator of mental stress.
Measuring
HR and HRV is a novel technique in wildlife research and has potential
for many new applications, including evaluating the impact of human
disturbance on large carnivores [12].
Cardiac-monitoring indicators can provide a mechanistic or functional
understanding of the behavioral effects of human disturbance on brown
bears, as suggested by the alteration of bear behavior when confronted
by people and human activities. In this study we used year-round HR and
HRV measurements to explore whether brown bears show a stress reaction
in relation to human settlements and thus if a human-induced landscape
of fear exists for brown bears using human-dominated areas.
2. Methods
2.1. Study area
The
study area was in southcentral Sweden. Elevations range from 200 to
1000 m above sea level, with most of the area below the timberline (c.
750 m). The hilly landscape is mostly covered with intensively managed
forest, dominated by Scots pine (Pinus silvestris) and Norway spruce (Picea abies). Heather, grasses, and berry-producing shrubs dominate the understory layer. Human density ranges from 4 to 7 habitants/km2. Logging, berry picking, fishing and hunting, including bear hunting, are common human activities in the area.
2.2. Preberry and berry seasons in relation with bear behavior and human activities
Brown
bears hibernate during winter, and the first period of bear activity
after leaving the den in spring includes the mating season. The major
foraging season, or hyperphagia, when bears eat primarily berries to
accumulate fat for hibernation, is from mid-July to den entry in October
[17].
In this study we used data from the annual active period of the bears,
divided into a preberry season (early April to < 15 July) and a berry
season (≥ 15 July to 31 October). This division has been used before to
study brown bear behavior in the same study area [29], [34] and [36] and elsewhere (e.g., [19]).
