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For Review Only
Evolutionary and ecological traps for brown bears in
human-modified landscapes
Journal:
Mammal Review
Manuscript ID
MAMMAL-17-67.R2
Manuscript Type:
Review
Keywords :
ecological traps, evolutionary traps, maladaptive choice, Ursus arctos,
source-sink
Subject Areas (select one):
Conservation/management
Mammalian Orders (select all
that apply):
Carnivora
Unreviewed manuscript
Evolutionary and ecological traps for brown bears in human-
modified landscapes
Vincenzo Penteriani* Research Unit of Biodiversity (UMIB, UO-CSIC-PA), Oviedo
University - Campus Mieres, 33600 Mieres, Spain, and Instituto Pirenaico de Ecología,
C.S.I.C., Avda. Nuestra Señora de la Victoria 16, 22700 Jaca, Spain. E-mail:
penteriani@ebd.csic.es
María del Mar Delgado Research Unit of Biodiversity (UMIB, UO-CSIC-PA), Oviedo
University - Campus Mieres, 33600 Mieres, Spain. E-mail: delgado.mmar@gmail.com
Miha Krofel Department of Forestry and Renewable Forest Resources, Biotechnical
Faculty, University of Ljubljana, Večna pot 83, SI-1001 Ljubljana, Slovenia. E-mail:
miha.krofel@gmail.com
Klemen Jerina Department of Forestry and Renewable Forest Resources, Biotechnical
Faculty, University of Ljubljana, Večna pot 83, SI-1001 Ljubljana, Slovenia. E-mail:
klemen.jerina@gmail.com
Andrés Ordiz Faculty of Environmental Sciences and Natural Resource Management,
Norwegian University of Life Sciences, Postbox 5003, NO–1432 Ås, Norway. E-mail:
andres.ordiz@gmail.com
Fredrik Dalerum Research Unit of Biodiversity (UMIB, UO-CSIC-PA), Oviedo University -
Campus Mieres, 33600 Mieres, Spain; Department of Zoology, Stockholm University,
10691 Stockholm, Sweden and Mammal Research Institute (MRI), Department of
Zoology and Entomology, University of Pretoria, Private Bag X20, Hatfield, 0028 South
Africa. E-mail: dalerumjohan@uniovi.es
Alejandra Zarzo-Arias Research Unit of Biodiversity (UMIB, UO-CSIC-PA), Oviedo
University - Campus Mieres, 33600 Mieres, Spain. E-mail: alejandra.zarzo@gmail.com
Giulia Bombieri Research Unit of Biodiversity (UMIB, UO-CSIC-PA), Oviedo University -
Campus Mieres, 33600 Mieres, Spain. E-mail: giulipan91@gmail.com
* Corresponding author: penteriani@ebd.csic.es
Acknowledgements
MMD was funded by a Spanish ‘Ramón y Cajal’ contract (nº RYC-2014-16263). KJ and
MK were supported by the Slovenian Research Agency (J4-7362, P4-0059).
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1
Evolutionary and ecological traps for brown bears in
1
human-modified landscapes
2
Abstract
3
1. Evolutionary traps, and their derivative, ecological traps, occur when
4
animals make maladaptive choices based on seemingly reliable
5
environmental cues and are important mechanistic explanations for
6
declines in animal populations.
7
2. Despite the interest in large carnivore conservation in human-modified
8
landscapes, the emergence of traps and their potential effects on the
9
conservation of large carnivore populations has frequently been
10
overlooked.
11
3. The brown bear Ursus arctos typifies the challenges facing large
12
carnivore conservation and recent research has reported that this
13
species can show maladaptive behaviours in human-modified
14
landscapes. Here we review, describe and discuss scenarios recognised
15
as evolutionary or ecological traps for brown bears, and propose possible
16
trap scenarios and mechanisms that have the potential to affect the
17
dynamics and viability of brown bear populations.
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4. Six potential trap scenarios have been detected for brown bears in
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human-modified landscapes: (1) food resources close to human
20
settlements; (2) agricultural landscapes; (3) roads; (4) artificial feeding
21
sites; (5) hunting; and (6) other leisure activities. Because these traps are
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likely of contrasting relevance for different demographic segments of
23
bear populations, we highlight the importance of evaluations of the
24
relative demographic consequences of different trap types for wildlife
25
management.
We also suggest that traps may be behind the decreases
26
of brown bear and other large carnivore populations in human-modified
27
landscapes.
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Key words: ecological traps, evolutionary traps, maladaptive choice, source-
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sink, Ursus arctos
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Running head: Brown bears and evolutionary/ecological traps
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Word count: 9,998
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Introduction
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Humans are currently one of the most important biotic forces on Earth (Palumbi
34
2001), as they have transformed nearly every landscape at unprecedented
35
rates and extents (Vitousek et al. 1997). Main and/or synergistic effects of
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resource exploitation, habitat destruction and fragmentation alter animal
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foraging ecology and behaviour. Anthropogenic impacts on habitats and animal
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populations are resulting in worldwide species range contractions and
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population decreases (e.g., Laliberte and Ripple 2004, Cardillo et al. 2005,
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Stoner et al. 2013, Fleschutz et al. 2016). This phenomenon is particularly
41
critical for large carnivores, whose widespread decline in numbers and
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distribution may also have cascading effects on the loss of global biodiversity
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(Ordiz et al. 2013, Ripple et al. 2014a).
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Animals base their habitat selection on physical characteristics of the
45
environment (settlement cues) that typically reflect habitat quality, e.g., food
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availability, mating opportunities, pressure from predators, as well as
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interspecific and intraspecific competition (Kristan 2003, Schlaepfer et al. 2002).
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Thus, an individual can base its habitat selection on sound ecological cues but,
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due to human interferences, these cues may no longer provide the expected
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fitness effects (Fletcher et al. 2012, Hale et al. 2015; Figure 1). In human-
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modified landscapes (also frequently described as human-dominated
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landscapes), evolutionary and ecological traps are important factors in the
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decline of animal populations (Schlaepfer et al. 2002, Robertson et al. 2013,
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Hale and Swearer 2016). Evolutionary traps, i.e., maladaptive behavioural
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choices made regardless of the availability of better options, and an important
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derivative of them, ecological traps, i.e., maladaptive habitat selection choices
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made despite the availability of better habitat, occur when animals make these
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choices based on seemingly reliable environmental cues, which an animal uses
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to presumably maximize its expected fitness (Battin 2004a, Robertson et al.
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2013, Schlaepfer et al. 2002). Ecological traps are thus subsumed by
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evolutionary traps because habitat selection can be considered a specific case
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of a behavioural choice where a given habitat is considered equally or more
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attractive than others, despite its lower fitness value. Moreover, to have
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persistent effects at the population level, individuals should move from source
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habitats into the ecological trap (Robertson & Hutto 2006, Lamb et al. 2017). A
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scenario where environmental cues do not match up with expectations of future
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fitness can occur through human modification of landscapes or even naturally,
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i.e., traps can also occur in pristine areas (Battin, 2004b). These habitat
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alterations engender the emergence of traps resulting from either (a) attraction
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for low-fitness options, (b) degraded fitness opportunities without a concomitant
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decrease in preference or (c) both attraction and degradation simultaneously
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(Sih et al. 2011, Robertson et al. 2013) (Figure 1).
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Traps are arguably an inevitable consequence of human-induced
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environmental change, because human alteration of the landscape may occur
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faster than cues that are shaping individual responses to the landscape can
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evolve (Hale and Swearer 2016, Robertson et al. 2013). Traps may also occur
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at a variety of scales (Battin 2004b, Hale & Swearer 2016), from landscape and
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within-patch levels, including edge effects at the boundary of protected areas
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(Loveridge et al. 2017), to small-scale site selection, such as the selection of
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dens and feeding sites. Traps differ from demographic sinks of classical source-
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sink systems because individuals occupy trap areas before or at the same time
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as high-quality habitats, whereas animals settle in sinks only when all higher-
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quality habitats are occupied (Battin 2004b). That is, individuals may select for
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traps, whereas sinks are not attractive or are even avoided. Distinguishing traps
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from source-sink systems is a priority in conservation biology, as sinks that are
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actually traps may attract a considerable portion of the source population and
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lead to overall population decrease or even extinction (Delibes et al. 2001,
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Gilroy and Sutherland 2007, Kokko and Sutherland 2001, Kristan 2003).
Early
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detection of traps is also important because the identification of apparently
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favourable habitats is an important step in conservation, and overlooking the
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possibility that apparently high-quality habitats may represent traps, can lead to
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detrimental management decisions (van der Meer et al. 2013, 2015).
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However, few studies have identified traps for mammals (Schlaepfer et
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al. 2002, Robertson & Hutto 2006, Hale & Swearer 2016), and even less for
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large carnivores (Loveridge et al. 2017, Pitman et al. 2015, Balme et al. 2010,
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van der Meer et al. 2013). Despite the interest in large carnivore conservation in
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human-modified landscapes, the emergence of traps and their potential effects
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on the conservation of large carnivore populations has frequently been
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overlooked. Trap effects are potentially worse in large carnivores than in any
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other group of species because larger carnivores have slow life histories, low
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densities and small population sizes, and they roam over wide home ranges
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(Ripple et al. 2014b).
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The brown bear as a model species
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The brown bear Ursus arctos illustrates well the challenges facing large
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carnivore conservation: an extensive species/population distribution range in
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combination with wide-ranging individual movements dictate that management
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of this species involves different spatial scales and heterogeneous habitats
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(Penteriani et al. in press). Despite a relatively wide distribution, brown bears
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are selecting particular habitats at various scales, from the landscape level to
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very fine scales (Nellemann et al. 2007, Ordiz et al. 2011). This may create
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conditions for the development of maladaptive behaviour in human-modified
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landscapes, even if substantial variation in this hierarchical habitat selection has
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the potential to create escape routes out of maladaptive behaviours. Like most
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large carnivores, brown bears are frequently involved in conflicts related to
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human safety, damages to crops and livestock depredation, often leading to the
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retaliatory killing of problem individuals (Can et al. 2014, Darimont et al. 2015).
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In human-modified landscapes bear habitats commonly juxtapose with those
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favoured by humans, where the frequency and lethality of contact between
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bears and humans likely increases (Mattson & Merrill 2002). As apex
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consumers, brown bears are highly vulnerable to traps because they do not
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have any natural predators, at least when they are adult individuals. This may
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reduce their vigilance in the face of a novel human threat. Bears adjust daily
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activity patterns and habitat choice to avoid hunting pressure (Ordiz et al. 2011,
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2012), and human settlements and human activities may have a stress effect on
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bears (Støen et al. 2015). However, bears may not be able to completely avoid
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novel human threats, which may lead to maladaptive behaviour in human-
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modified landscapes (Lamb et al. 2017). The interest in brown bears as a model
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species is also justified because they are hunted for sport across most of their
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Holarctic distribution range. Bear survival is often reduced in areas closer to
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human settlements and infrastructures, and this pattern holds for both North
131
America (Lamb et al. 2017) and Europe (Steyaert et al. 2016b).
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Here we review, describe and discuss scenarios that have been
133
recognised as evolutionary or ecological traps for brown bears, and propose
134
possible trap scenarios and mechanisms that have the potential to affect the
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dynamics and viability of brown bear populations over their distribution range in
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the near future (Table 1). This information is useful to forecast potential
137
hotspots of conservation and management interest (Figure 1).
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Methods
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To select articles for our review, we used Google Scholar and Thomson
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Reuters ‘Web of Science’ databases. We conducted the literature review
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(summer 2017) using a broad range of search terms that represent the variety
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of ways in which both ‘traps’ and ‘brown bear’ may be included. Thus, the terms
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‘bear’ and ‘grizzly’ were combined with the following terms (in alphabetical
145
order): ‘ecological trap’, ‘evolutionary trap’, ‘maladaptive’, ‘source-sink’ and
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‘trap’. We also searched in the literature-cited sections of all recorded articles.
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Ideally, to demonstrate a trap mechanism on animal fitness, studies should take
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into account both survival and reproduction, as they can have offsetting effects
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on the severity of a trap or its existence. To be conservative and given that the
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reproductive component of fitness was often ignored in the reviewed bear
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studies, which mostly focused and/or demonstrated effects on bear survival
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(e.g., increased mortality rates), we always refer to suggested traps as potential
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traps.
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Results
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Human settlements, abundant food and the possible emergence of
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ecological traps
158
Because of the high nutritional demands of the grizzly (brown) bear, areas with
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attractive food (natural or anthropogenic) close to human settlements create the
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conditions for the emergence of an ecological trap bears in the Canadian Rocky
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Mountains (Lamb et al. 2017). Indeed, when abundant resources occur in the
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vicinity of humans, anthropogenic mortality (e.g., hunting, management
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removals due to conflicts with humans, road and railway collisions, and
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poaching; Gangadharan et al. 2017, Lamb et al. 2017) represents the primary
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cause of mortality in bears. In the absence of humans, consuming high-energy
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berries benefits grizzly bears’ fitness (McLellan 2011, 2015, Welch et al. 1997),
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thus representing an attraction for them (McLellan and Hovey 2001, Nielsen et
168
al. 2010, 2003). However, presence of highly attractive habitat patches in close
169
proximity to human settlements created a trap scenario (Robertson et al. 2013,
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Hale et al. 2015), which intensified demographic loss in source populations.
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Increased mortality and food associated with proximity to human settlements:
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(1) caused a bear population decline of ̴8% per year inside and 1.5% outside
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the trap area; (2) reduced survival and compensation in recruitment to prevent
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population decline; and (3) caused an immigration of individuals into the trap
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area from contiguous locations at a ratio of ten bears entering the trap and
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dying for every bear leaving the trap and dying. Lamb et al. (2017) also showed
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another crucial facet of this trap mechanism, which worsens the severity of the
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trap: bear mortality was mainly due (68%) to non-hunting sources of human-
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caused mortality (e.g., collisions with vehicles and trains, illegal kills), a mortality
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source that cannot be mitigated through regulatory policies, as is done with
181
hunting.
182
The combination of highly attractive food resources and high
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anthropogenic mortality creates unoccupied spaces that primarily are
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recolonised by young (mainly male) dispersers. Individuals killed in the trap
185
area were on average three years younger than those killed outside (Lamb et
186
al., 2017). This age and sex-skewed composition of the individuals in these trap
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areas suggests that dispersing juvenile males are the best candidates to occupy
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vacant risky areas. In areas with few females and many young males the
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reproductive potential of the population is low (Lamb et al. 2017). Attractive food
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may provide little motivation for dispersers to move out of the trap area, and the
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longer bears stay in the trap, the more likely they are to be killed by humans. On
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the other hand, if the trap is an apparently suitable area, younger bears may not
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be motivated to move into other areas with fewer human settlements where
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competition for mates, food and space may confront them with older bears
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inhabiting safer areas (Nellemann et al. 2007). This type of trap has the
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potential to have severe demographic consequences for slowly reproducing
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species like the brown bear (Table 1).
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Finally, emigrations out of a declining population because of the effect of
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an ecological trap may create severe conservation problems if source
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populations are small and the landscapes in which the trap is acting are
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exceptionally attractive (Lamb et al. 2017). Because of the large home ranges
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of brown bears and the movement of young individuals, the effects of localised
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mortality in a trap area might result in negative demographic consequences for
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areas far from traps (Table 1). Thus, addressing these subtle and insidious
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sources of mortality is an essential step for the long-term viability of bear
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populations, which also highlights the need to maintain the quality of
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undamaged landscapes that can provide safe refuge from human expansion
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and associated human–bear conflicts (Lamb et al. 2017).
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Agricultural landscapes as ecological traps
210
Agricultural lands represent an extremely conflictual human-modified landscape
211
for bears, where they compete with humans for space and resources, resulting
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in conflicts that frequently end in damage to human property, bears being killed
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in defence of life or property, government-supported reduction of bear
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populations and bear relocations (Wilson et al. 2005, 2006, Northrup et al.
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2012b). In southwestern Alberta, Canada, bear–human conflicts resulted from
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overlaps in human settlements and agricultural practices with grizzly bear
217
preferred habitats (Northrup et al. 2012b). In this potential trap scenario, where
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landscapes preferred by bears directly overlapped with areas of high conflict
219
risk, conflicts were more likely to occur in areas with higher human density and
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vehicle access. The identification of these areas was an essential step in
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conflict reduction because bears selected private agricultural lands: over the
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50% of them were considered as ecological traps at night, when the individuals
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were most active (Northrup et al. 2012b). Agricultural landscapes may become
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traps principally when bears were attracted to anthropogenic foods, such as
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dead cattle and grain storage containers (Mattson & Merrill 2002, Wilson et al.
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2005, 2006).
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Steyaert et al. (2016b) revealed a similar mechanism in central Sweden,
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where nutritious oat crops attract bears and expose them to a higher hunting
229
risk compared to non-agricultural habitats. Up to 8.4% of the bears were killed
230
in agricultural lands, although these areas covered <0.5% of the study area and
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only 1% of all bear GPS fixes were recorded within that land cover type, i.e.,
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bear mortality risk was larger near villages, roads, buildings, and agricultural
233
grounds than in the more utilized forest habitat surrounding agricultural lands
234
(Steyaert et al., 2016b). This showed that mortality risks are not homogenously
235
distributed throughout the landscape, but they are much higher in areas with
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human activities, like agricultural fields.
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Both Northrup et al. (2012) and Steyaert et al. (2016b) contend that it is
238
crucial to identify potential ecological traps and how they work, to be able to
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focus on effective mitigation efforts in such areas. Once identified, agricultural
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stakeholders can be involved in management policies to ensure implementation
241
of husbandry practices that limit potential conflicts, e.g., proper storage of
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attractants, grazing of cattle in lower-risk areas and improved livestock
243
protection (Northrup et al. 2012b, Treves et al. 2016). Trap identification and
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localization is facilitated by the availability of geo-referenced bear mortality and
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human-bear interaction data, preferably over long periods.
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Roads as potential ecological traps
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The ecological effects of roads represent a pressing issue in animal
248
conservation (Trombulak & Frissel 2000), and bears are no exception among
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affected species (e.g., Bischof et al. 2017, Skuban et al. 2017, Lamb et al.
250
2018). Roads fragment habitats and can affect bear behaviour, survival,
251
reproduction and population viability (Northrup et al. 2012a, Boulanger &
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Stenhouse 2014, Skuban et al. 2017). Moreover, the relationship between
253
roads and bears can be complex because road effects may often be area-
254
and/or sex-specific, vary by time of day and season, and be affected by traffic
255
volume. One of the principal factors that have reduced brown bear populations
256
in some areas of North America has been the effects of high mortality related to
257
the human access into bear habitat by roads (Schwartz et al. 2006, Boulanger &
258
Stenhouse 2014). Nielsen et al. (2006) and Northrup et al. (2012a) suggested
259
that roads may cause habitat loss, alter movement patterns and, consequently,
260
can become ecological traps for brown bears. For example, proximity to roads
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with high traffic volume might increase nutritional and psychological stress,
262
whereas displacement from better areas can determine substantial energy loss
263
(Nielsen et al. 2006, Northrup et al. 2012a). These kinds of behavioural
264
responses could decrease productivity at the population level (Northrup et al.
265
2012a).
As evidence of the possibility that roads may become bear ecological
266
traps, Boulanger and Stenhouse (2014) demonstrated that in Alberta, Canada,
267
sex and age class survival was associated with road density, as subadult bears
268
were the most exposed to road-based mortality, and females with cubs-of-the-
269
year and/or yearlings had lower survival than females with two year olds or no
270
cubs at all. Frequent bear mortality near roads was also demonstrated by
271
McLellan (2015). Indeed, most fatalities may occur near roads from which bears
272
are killed (Mace et al. 1996, McLellan 2015) and new roads may increase the
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number of bears poached: bigger road networks could improve the
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effectiveness of poachers searching for bears (McLellan 2015). Additionally,
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roads may fragment bear populations as a result of the high mortality around
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roads (Proctor et al. 2012, Boulanger & Stenhouse 2014, Skuban et al. 2017).
277
A possible mechanism of roads acting as ecological traps could be the
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attraction of females with cubs-of-the-year to roads due to higher forage
279
availability (e.g., increasing the risk of bears getting killed in vehicle collisions;
280
see also Northrup et al. 2012a) or as an avoidance mechanism against
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potentially infanticidal adult males, which generally avoid the vicinity of roads
282
(Boulanger and Stenhouse 2014). Thus, females with cubs are attracted to
283
areas close to roads despite higher mortality rates. As mentioned previously,
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such a trap mechanism may have serious demographic consequences,
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although the net negative effects of road kill versus juvenile mortality caused by
286
sexually selected infanticide (SSI, i.e., a reproductive strategy of
males that can
287
increase their fitness by killing unrelated offspring so as to bring a female into
288
reproductive condition and, thus, increase the chance of the infanticidal male to
289
subsequently reproduce with her; Hrdy 1979) need to be evaluated. Also, bears
290
often choose to forage along roadsides in spring (Nielsen et al. 2002), which
291
highlights a probable mismatch between perceived habitat quality and real
292
fitness benefits. Important to note is that even if brown bears exhibit a despotic
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social organization where adult males may influence the habitat choices of
294
females with cubs (due to the risk they pose due to SSI; Nellemann et al. 2007,
295
Elfström et al. 2014) and cause females with cubs to select areas closer to
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roads more often than other bears, displacements of females with cubs
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triggered by adult males should not necessarily determine the entrance of bear
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families in a trap.
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Road development in critical bear areas should thus be limited under
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specific, local thresholds (Nielsen et al. 2006, Boulanger & Stenhouse 2014,
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Lamb et al. 2018) or require strict control of human access, as well as the
302
deactivation and re-vegetation of roads in areas requiring the temporary
303
extraction of resources (Nielsen et al. 2006). Additionally, the spatial distribution
304
of individuals should be coupled with measures of road densities and use to
305
evaluate land management decisions (Boulanger & Stenhouse 2014, Ordiz et
306
al. 2014, Skuban et al. 2017).
307
It is worth noting here that railways can also negatively impact bears as
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they clearly visit railways to obtain food, but can be killed by trains. For
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example: (a) in Slovenia ca. 40% of all bear traffic mortality is caused by
310
railways, e.g., when bears are searching for the carrion of railway-killed
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ungulates (Kaczensky et al. 2003, Krofel et al. 2012); and (b) the large amount
312
of grain that spills from trains passing through Banff and Yoho National Parks,
313
Canada, attract grizzlies and contribute to increase the number of bear–train
314
collisions (Gangadharan et al. 2017).
315
Artificial feeding as a potential evolutionary trap mechanism
316
Artificial feeding of bears, i.e., baiting for hunting or viewing purposes and
317
diversionary feeding for diverting bears from human settlements, is
318
controversial, because it can alter movement patterns and the spatial
319
distribution of individuals, their feeding behaviour and preferences, denning
320
ecology, and interspecific interactions (Selva et al. 2017, Oro et al. 2013, Krofel
321
& Jerina 2016, Kirby et al. 2017, Krofel et al., 2017, Penteriani et al. 2017).
322
Moreover, physiological problems may be expected when supplementary food
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is not appropriate for bears (Penteriani et al. 2010, 2017); e.g., bait for hunting
324
may consist of high-calorie foods, which can include high-sugar foods, such as
325
cookies, donuts and candies (Kirby et al. 2017). Artificial feeding could also
326
affect bear nutrition through increased body size and energy requirements, as
327
observed in grizzly bears foraging on garbage dumps (Robbins et al. 2004).
328
In many countries, especially in Europe, artificial feeding of bears is
329
recommended or even compulsory (Kavčič et al. 2013, 2015). This
330
management measure should, among other purposes, divert the bears from
331
people and thus decrease conflict rates. Conversely, the feeding of bears is
332
strongly discouraged or even forbidden in other parts of the world, especially in
333
North America (Kavčič et al. 2013, Garshelis et al. 2017). It is commonly
334
believed that bears that associate artificial feeding with people lose their natural
335
caution and often become a nuisance (Kavčič et al. 2013). Recent studies
336
indicate that artificial feeding in different natural and management settings may
337
increase, not affect, or decrease conflict rates (Kavčič et al. 2013, Steyaert et al.
338
2014, Stringham & Bryant 2015, Bautista et al. 2016, Garshelis et al. 2017,
339
Morehouse & Boyce 2017). This is likely caused by a number of factors, such
340
as annual or seasonal fluctuations of food availability, the spatial arrangement
341
of feeding sites, the type of artificial food and the way in which this food is
342
provided (e.g., hand feeding vs. automatic feeders), and probably also from the
343
intensity of bear hunting in relation to increased food availability (see Garshelis
344
et al. 2017 for synthesis). Moreover, well planned and regulated artificial feeding
345
in the framework of adaptive management can help decrease conflicts
346
(Garshelis et al. 2017) and maintain a higher density of bears, possibly leading
347
to sustainable species preservation.
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Moreover, artificial feeding, as observed for black bears Ursus
349
americanus, might: (a) contribute substantially to bear diets (Kirby et al. 2017);
350
(b) drive bears to increase their use of these developed areas according to
351
physiological demands for food (e.g., hyperphagia and natural food shortage
352
years; Baruch-Mordo et al. 2014, Johnson et al. 2015); and (c) induce females
353
to train their cubs to seek artificial foods (Mazur and Seher, 2008). Food from
354
artificial feeding sites can represent one of the most important food sources for
355
brown bears as well (Kavčič et al. 2015), and a large proportion of bears at least
356
occasionally use artificial feeding sites if these are available (Krofel & Jerina
357
2016). Bears may interpret food at artificial feeding sites as the best available
358
option and, thus, focus on it instead of preferring to forage for natural foods (but
359
see Jerina et al. 2012, 2015, Kavčič et al. 2015, for an opposite result at the
360
population level). This choice might potentially have negative effects on (a)
361
individual health and (b) cubs learning food habits, if the artificial feeding sites
362
are frequented by females with cubs (Penteriani et al. 2010, 2017). Additionally,
363
artificial feeding sites may artificially increase local bear density and/or increase
364
reproduction (Jerina et al. 2013), alter bear movements (Selva et al. in press)
365
and increase the frequency of interactions among the bears (Krofel et al. 2016),
366
which may engender intraspecific competition, aggressive encounters and
367
perhaps also infanticide risk (Ben-David et al. 2004). Thus, the use of feeding
368
sites may in certain settings represent a maladaptive behavioural choice,
369
because the artificial food is considered equally or more attractive than other
370
resources despite a lower fitness value in terms of survival, health and
371
behaviour, ensnaring individuals in a trap.
372
Hunting and ecological traps for females with cubs and young bears
373
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Bear hunting is not necessarily related or exclusive to human-modified
374
landscapes, but its practice is more frequent in those areas where human
375
densities are higher. Even though this leisure activity has never been evaluated
376
under the perspective of a trap mechanism, we propose here that bear hunting
377
might engender a subtle trap mechanism that determines maladaptive choices
378
based on seemingly reliable environmental cues by females with cubs.
379
The hunting of adult brown bear males can disrupt locally stable social
380
structures. When an adult male is removed, one or more immigrating males
381
replacing the dead individual may kill existing cubs in order to reproduce
382
(Swenson et al. 1997, Leclerc et al. 2017). Thus, the removal of adult males
383
through hunting can increase the risk of SSI. Besides the direct demographic
384
effects of hunting males, SSI increases cub mortality and as such can decrease
385
brown bear population growth (Swenson et al. 1997). Therefore, disruption of
386
the social structure may exacerbate the demographic effects of hunting (Table
387
1), increasing demographic variability and ultimately affecting population size
388
(Leclerc et al. 2017).
389
Hunting also has relatively wide spatial and temporal effects on bear
390
populations because: (a) the killing of an adult male has the potential to reduce
391
the survival of cubs within 25 km of the harvested male (Gosselin et al. 2017)
392
and, (b) by removing adult males from the population, hunters destabilize the
393
spatial organization of the population for at least two years after a male has
394
been killed (Leclerc et al. 2017).
395
Females with cubs avoid males during the mating season as a
396
counterstrategy to SSI (Dahle and Swenson 2003, Steyaert et al. 2013), e.g.,
397
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females avoid habitat types frequented by males and select for habitat close to
398
humans (Steyaert et al., 2016), which can have a negative effect on the quality
399
of their diet (Steyaert et al., 2013) and may reduce reproductive output (Wielgus
400
& Bunnell 2000). Therefore, by increasing the risk of SSI, hunting pressure
401
might trigger a trap mechanism which is additive to the effect of male
402
avoidance. That is, in areas where bear hunting is allowed, females already
403
settling in less favourable habitats due to the risk of infanticide might experience
404
an additional negative effect, i.e., the increased risk of SSI because of the
405
arrival of new individuals following the removal of resident males. The death of
406
resident males, which were the potential mates the year before den emergence
407
with cubs, and the consequent immigration of new males (the potential
408
infanticidal bears), can be two facets of a process relatively difficult to detect for
409
mother bears (Gosselin et al. 2017).
410
SSI in brown bears has been documented in different bear populations
411
(e.g., Palomero et al. 2007, Swenson et al. 1997, Wielgus et al. 1994), whereas
412
it seems to be less common or absent in some other bear ranges (McLellan
413
2005). Therefore, the potential effects of SSI on bear population growth rates
414
may vary among bear populations depending on local ecological and
415
evolutionary constraints. Accordingly, the role of bear hunting as an ecological
416
trap in relation to the occurrence of SSI and habitat selection of females with
417
cubs may also differ across the distribution range of the species.
418
Potential for other trap mechanisms
419
After centuries of persecution, human activities are likely perceived by bears as
420
a predation risk that oblige them to increase vigilance instead of foraging, e.g.,
421
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during the hunting season and the times of day when humans are in the forest
422
(Ordiz et al. 2011 and 2012). This trade-off suggests the presence of a human-
423
induced landscape of fear for large carnivores in human-modified landscapes
424
(Ordiz et al. 2013, Støen et al. 2015, Steyaert et al. 2016b). However, some
425
bear populations have come under hunting pressure relatively recently
426
(Zedrosser et al. 2011), while others have been under protection for decades,
427
e.g., brown bears in Spain and Italy, and simultaneously some human
428
recreational activities focusing on bears, i.e., ecotourism, have intensified lately.
429
An eventual reduction in the aversion to humans by large carnivores may
430
potentially create a trap, where animals that often face non-aggressive human
431
presence in their immediate surroundings, as it happens when bear populations
432
are subjected to bear-viewing activities (Penteriani et al. 2017), may face an
433
increased mortality risk. Indeed, losing fear to humans may increase bear
434
presence close to human settlements and infrastructures because of
435
habituation, i.e., the loss of human avoidance and escape responses (Smith et
436
al. 2005). Therefore, proper management of ecotourism practices is urgent (see
437
Penteriani et al. 2017).
438
Another human activity that has the potential to represent a trap
439
mechanism attracting bears to areas with potentially high mortality rates is the
440
reindeer husbandry of the Sámi people, the indigenous people of northern
441
Fennoscandia. The Sámi allow their reindeer herds to move across large
442
distances, in an area that covers approximately half of the area of Scandinavia,
443
for instance, overlapping with brown bears (Hobbs et al. 2012, Sivertsen et al.
444
2016). Reindeer calving grounds may attract bears because reindeer calve just
445
at the time when bears are emerging from winter dens and reindeer neonates
446
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can be an important component of the bear diet as bears are in a physiological
447
state in which they need protein (Sivertsen et al. 2016). In this context, due to
448
the high predation rates of bears on reindeer neonates (Sivertsen et al. 2016),
449
removal of bears increases to reduce predation, which decreases the number of
450
reindeer that can be harvested by the Sámi (Hobbs et al. 2012). This trap
451
mechanism may be exacerbated by human alteration of landscapes such as
452
forest harvesting and road construction. Indeed, effects of human-caused land-
453
use changes can influence reindeer–brown bear behavioural interactions and,
454
in turn, vulnerability to bear predation (Sivertsen et al. 2016). Suggested
455
mitigation measures to reduce bear predation include: (a) fencing, keeping
456
reindeer females in enclosures during calving and some weeks afterwards
457
(Hobbs et al. 2012), which may help to reduce bear attraction to reindeer
458
calving grounds; (b) zoning for carnivore conservation and reindeer herding in
459
different areas (Ordiz et al. 2017); and (c) minimizing forestry activities in the
460
main reindeer calving ranges in reindeer herding districts (Sivertsen et al.
461
2016).
462
463
Discussion
464
Beyond the interest of trap mechanisms for evolutionary and population
465
ecology, traps have clear conservation implications. It is crucial to pay attention
466
to habitat choices in bear populations, in order to recognise cases where a
467
mismatch between preferences and habitat quality could lead to population
468
declines. Because cue-response relationships in wild animals will be difficult to
469
change, increasing the actual quality of the trap area by decreasing the level of
470
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anthropogenic mortality is likely to be the best solution to mitigate the impact of
471
the trap or to transform it in a source area (van der Meer et al. 2013).
472
Thus, when managing potential trap habitats, it is crucial to consider the
473
habitat quality as perceived by individuals (Patten & Kelly 2010). Creating high-
474
quality habitats from previous traps without the right cues will be of little use,
475
while allowing poor-quality habitats to appear suitable might be damaging to the
476
entire population (Kokko & Sutherland 2001). As suggested by van der Meer et
477
al. (2015), the quality of the trap habitat guides the type of intervention (Figure
478
1), i.e., the type of interventions used to restore the trap will depend on the
479
target(s) of human disturbances: (a) if the habitat quality is high, human effects
480
need to be reduced to increase habitat suitability, which may turn the trap into a
481
source; otherwise, (b) if the habitat quality of the trap is low, but human
482
modification has increased its attractiveness, efforts should be made to reduce
483
trap attractiveness, which would turn it into a sink. Therefore, restricting human
484
access and/or modifying habitat quality to make areas where bears can easily
485
encounter humans less attractive or accessible to bears need to be considered
486
(Nielsen et al. 2006). In some cases such modifications will be difficult to
487
implement, but some (e.g., changes in artificial feeding regimes) could be done
488
relatively easily with adjustments in bear management.
489
Considering the possibility that brown bears may occupy exclusively
490
either source or trap habitats is unrealistic because of their large home ranges
491
(Schwartz et al. 2006). Actually, bears may include safe and trap areas within
492
their annual or life ranges (Knight et al. 1988). As highlighted by Schwartz et al.
493
(2006), survival for bears and the viability of bear populations are the result of
494
multiple survival probabilities, depending on the number, size and spatial
495
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locations of traps in the landscape contained within bear home ranges and the
496
amount of time each individual spends at any particular location in the
497
landscape. Additionally, landscape utilization is also dynamic because it
498
depends on the complex life cycle and social structure of brown bears.
499
Landscape use may change with seasons, food availability and distribution,
500
seasonal and long-term intra-specific interactions, e.g., during mating seasons
501
and owing to the spatial structure of individuals across the landscape depending
502
on their sex and age, and other environmental factors.
503
Fully understanding mortality risk for an individual requires information
504
about the likelihood that (a) mortality will occur at a given location and (b) the
505
animal will use this particular location, i.e., the level of exposure to that mortality
506
risk. For example, a high-risk location may either be one that is infrequently
507
visited by an individual, but where the likelihood of mortality is high, or one in
508
which the chance of dying is lower, but where an individual spends substantial
509
amounts of time (Loveridge et al. 2017). On the other hand, it is important to
510
note that studies on traps have almost exclusively focused on mortality, which is
511
just one component of individual fitness. When analysing the effects of traps on
512
animal populations, it is important to consider also the reproductive component
513
of fitness and how it could offset some of the negative effects of increased
514
mortality. Thus, trap identification can be costly, particularly if data on
515
reproduction, mortality and habitat selection is required to reliably identify a trap.
516
Additionally, bears might show adaptation to misleading cues over time through
517
the turnover of individuals falling in the trap. That is, over time individual
518
turnover may result in a population of individuals that are 'trap-averse' and that
519
are better at matching the right cues with fitness expectations. Indeed,
520
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individual variation is often overlooked in studies on trap mechanisms, which
521
prevalently use population-level parameters, but in situations with high inter-
522
individual variation in habitat selection (e.g., Leclerc et al. 2016, Lesmerises &
523
St-Laurent 2017), a trap is less likely to persist (Battin 2004b).
524
The removal of individuals from trap areas may also create vacancies,
525
attracting new individuals from neighbouring regions. This ‘vacuum effect’ has
526
already been documented in carnivores and may cause edge effects to extend
527
within large protected areas (Balme et al. 2010). For example, hunting along
528
park boundaries generated territorial vacuums that were filled by the
529
immigration of male lions Panthera leo from the protected area (Loveridge et al.
530
2007, 2009, 2017). Hunting areas are therefore typical ecological traps with
531
both a high level of use and a high risk of mortality that may lead to maladaptive
532
habitat selection by large carnivores. For lions, this occurred because these
533
areas contained relatively intact habitat, good prey populations, and low human
534
presence, which did not present the obvious cues to trigger avoidance.
535
However, if hunting mortality hot spots across the landscape are sustainably
536
managed (with sustainable hunting quotas and rigorous monitoring of
537
populations), they may both ensure the conservation of intact natural habitat
538
important for wildlife and play a crucial role as buffer areas around protected
539
areas (Loveridge et al. 2017).
540
Although protected areas have been crucial for the conservation of brown
541
bears in the United States, most bears in North America live outside of
542
protected areas, where human growth across landscapes is increasing
543
(McLellan, 2015). Even in the lower 48 US states, brown bears are increasing
544
out of protected areas and it is expected that future bear distribution will largely
545
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overlap with human-modified landscapes (McLellan, 2015). Similar trends are
546
observed in Europe as a result of the continuous increase of the species in
547
some human-modified lands (Chapron et al., 2014). As noted above, traps of
548
anthropogenic origin are largely connected with human activities outside
549
protected areas. Thus, for effective brown bear conservation, it is important to
550
know how, when and where traps may arise and what factors may have a
551
negative influence on bears both inside and outside of protected areas. Zones
552
outside protected areas frequently represent population traps because of
553
humans killings, and most deaths occur beyond park boundaries, mainly when
554
reserves are small relative to bear home ranges (Schwartz et al. 2006). Similar
555
dynamics may occur when bear populations are shared by several countries,
556
where they are exposed to different management regimes (Penteriani et al. in
557
press).
558
Negative consequences of traps are exacerbated when safe areas are
559
small, with lower habitat suitability and higher human densities than traps. The
560
worldwide increase of the human population has intensified fragmentation of
561
habitats available to wide ranging large carnivores (Crooks et al. 2017),
562
frequently constraining animals to live in closer vicinity to humans (Woodroffe
563
2000, Inskip & Zimmermann 2009). By crossing into non protected areas,
564
animals generally come closer to humans and may be accidentally or
565
deliberately killed by them (van der Meer et al. 2013). Although this may
566
suggest that protected areas may offer little conservation value, research on
567
cougars Puma concolor has shown that, when human-mediated mortality is
568
widespread, safe areas may harbour carnivore populations and may have
569
greater conservation value than previously supposed (Stoner et al. 2013).
570
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Similar trap scenarios have also been detected for other carnivores. Leopards
571
Panthera pardus in the Limpopo Province, South Africa, and African wild dogs
572
Lycoan pictus in Hwange National Park, Zimbabwe, select high-quality habitat
573
within buffer zones of protected area, which is likely maladaptive due to the
574
fitness costs associated with the increasing risk of human-induced mortality in
575
farming areas (where the likelihood of conflict is high; Balme et al. 2010, Pitman
576
et al. 2015, van der Meer et al. 2013). Indeed, trap areas put apparently safe
577
populations close to sources of human-mediated mortality: fitness-enhancing
578
favourable ecological conditions attract individuals unable to perceive the higher
579
mortality risk posed by humans (e.g., road traffic and shooting).
580
Despite (1) the potential of human-modified landscapes as primary areas
581
for trap occurrence, (2) the number of scenarios that may trigger the emergence
582
of traps and, (3) the crucial importance of recognizing traps for brown bear
583
conservation and management, the trap mechanisms, locations and effects are
584
still largely overlooked and more information on demographic effects and the
585
reproductive side of fitness is required. This lack of knowledge may engender
586
serious negative consequences on bear populations worldwide and reduce the
587
effectiveness of conservation actions because trap mechanisms are frequently
588
subtle and difficult to distinguish. If not detected promptly, conservation
589
practices may not be implemented in time to reverse the fate of individuals and
590
populations. There are several brown bear populations that remain
591
understudied and, given that brown bears are long-lived, long-term studies will
592
be required to see if traps are severe enough to realistically endanger
593
populations, especially those that are under hunting pressure or in areas
594
characterised by landscape change. More effort should thus be put into the
595
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consideration that traps may be behind the unexpected decreases of brown
596
bear and other large carnivore populations in human-modified landscapes.
597
Focusing research on this topic will help forecast potential hotspots for
598
carnivore conservation and management in a global scenario of increasing
599
human populations and partial carnivore recoveries.
600
601
References
602
Balme GA, Slotow R, Hunter LTB (2010) Edge effects and the impact of non-
603
protected areas in carnivore conservation: Leopards in the Phinda-Mkhuze
604
Complex, South Africa. Animal Conservation 13: 315–323.
605
Baruch-Mordo S, Wilson KR, Lewis DL, Broderick J, Mao JS, Breck SW (2014)
606
Stochasticity in natural forage production affects use of urban areas by black
607
bears: implications to management of human-bear conflicts. PLoS ONE 9: 1–
608
10.
609
Battin J (2004a) Bad habitats: Animal ecological traps and the conservation of
610
populations. Society for Conservation Biology 18: 1482–1491.
611
Battin J (2004b) When good animals love bad habitats: Ecological traps and the
612
conservation of animal populations. Conservation Biology 18: 1482–1491.
613
Bautista C, Naves J, Revilla E, Fernández N, Albrecht J, Scharf AK et al. (2016)
614
Patterns and correlates of claims for brown bear damage on a continental scale.
615
Journal of Applied Ecology 54: 282–292.
616
Ben-David M, Titus K, Beier L (2004) Consumption of salmon by Alaskan brown
617
Page 26 of 43Unreviewed manuscript
For Review Only
27
bears: a trade-off between nutritional requirements and the risk of infanticide?
618
Oecologia 138: 465–474.
619
Bischof R, Steyaert SMJG, Kindberg J (2017) Caught in the mesh: Roads and
620
their network-scale impediment to animal movement. Ecography: 1–12.
621
Boulanger J, Stenhouse GB (2014) The impact of roads on the demography of
622
grizzly bears in Alberta. PLoS ONE 9: 1–22.
623
Can ÖE, D’Cruze N, Garshelis DL, Beecham J, Macdonald DW (2014)
624
Resolving Human-Bear Conflict: A Global Survey of Countries, Experts, and
625
Key Factors. Conservation Letters 7: 501–513.
626
Cardillo M, Mace G, Jones K, Bielby J, Bininda-Emonds, O Sechrest W, Orme
627
C, Purvis A (2005) Multiple causes of high extinction risk in large mammal
628
species. Science 309: 1239–1241.
629
Chapron G, Kaczensky P, Linnell JDC, von Arx M, Huber D, Andren H et al.
630
(2014) Recovery of large carnivores in Europe’s modern human-dominated
631
landscapes. Science 346: 1517–1519.
632
Crooks KR, Burdett CL, Theobald DM, King SRB, Di Marco M, Rondinini C,
633
Boitani L (2017) Quantification of habitat fragmentation reveals extinction risk in
634
terrestrial mammals. Proceedings of the National Academy of Sciences:
635
201705769.
636
Dahle B, Swenson JE (2003) Seasonal range size in relation to reproductive
637
strategies in brown bears Ursus arctos. Journal of Animal Ecology 72: 660–667.
638
Darimont CT, Fox CH, Bryan HM, Reimchen TE (2015) Human impacts: The
639
Page 27 of 43 Unreviewed manuscript
For Review Only
28
unique ecology of human predators. Science 6250: 858–860.
640
Delibes M, Ferreras P, Gaona P (2001) Attractive sinks, or how individual
641
behavioural decisions determine source-sink dynamics. Ecology Letters 4: 401–
642
403.
643
Elfström M, Zedrosser A, Jerina K, Støen OG, Kindberg J, Budic L, Jonozovič
644
M, Swenson JE (2014) Does despotic behavior or food search explain the
645
occurrence of problem brown bears in Europe? Journal of Wildlife Management
646
78: 881–893.
647
Fleschutz MM, Gálvez N, Pe’er G, Davies ZG, Henle K, Schüttler E (2016)
648
Response of a small felid of conservation concern to habitat fragmentation.
649
Biodiversity and Conservation 25: 1447–1463.
650
Fletcher RJ, Orrock JL, Robertson BA (2012) How the type of anthropogenic
651
change alters the consequences of ecological traps. Proceedings of the Royal
652
Society B-Biological Sciences 279: 2546–2552.
653
Gangadharan A, Pollock S, Gilhooly P, Friesen A, Dorsey B, St. Clair CC (2017)
654
Grain spilled from moving trains create a substantial wildlife attractant in
655
protected areas. Animal Conservation: 391–400.
656
Garshelis DL, Baruch-Mordo S, Bryant A, Gunther KA, Jerina K (2017) Is
657
diversionary feeding an effective tool for reducing human–bear conflicts? Case
658
studies from North America and Europe. Ursus 28: 31–55.
659
Gilroy JJ, Sutherland WJ (2007) Beyond ecological traps: perceptual errors and
660
undervalued resources. Trends in Ecology and Evolution 22: 351–356.
661
Page 28 of 43Unreviewed manuscript
For Review Only
29
Gosselin J, Leclerc M, Zedrosser A, Steyaert SMJG, Swenson JE, Pelletier F
662
(2017) Hunting promotes sexual conflict in brown bears. Journal of Animal
663
Ecology 86: 35–42.
664
Hale R, Swearer SE (2016) Ecological traps : current evidence and future
665
directions. Proceedings of the Royal Society B 283: 20152647.
666
Hale R, Treml EA, Swearer SE (2015) Evaluating the metapopulation
667
consequences of ecological traps. Proceedings of the Royal Society B:
668
Biological Sciences 282: 20142930–20142930.
669
Hobbs NT, Andrén H, Persson J, Aronsson M, Chapron G (2012) Native
670
predators reduce harvest of reindeer by Sámi pastoralists. Ecological
671
Applications 22: 1640–1654.
672
Hrdy B (1979) Infanticide among animals: a review, classification, and
673
examination of the implications for the reproductive strategies of females.
674
Ethology and Sociobiology 1: 13–40.
675
Inskip C, Zimmermann A (2009) Human–felid conflict: a review of patterns and
676
priorities worldwide. Oryx 43: 18–34.
677
Jerina K, Jonozovič M, Krofel M, Skrbinšek T (2013) Range and local
678
population densities of brown bear Ursus arctos in Slovenia. European Journal
679
of Wildlife Research 59: 1–9.
680
Jerina K, Krofel M, Mohorović M, Stergar M, Jonozovič M, Seveque A (2015)
681
Analysis of occurrence of human–bear conflicts in Slovenia and neighbouring
682
countries. University of Ljubljana, Biotechnical Faculty, Department of Forestry
683
and Renewable Forest Resources, Nature project LIFE13 NAT/SI/000550.
684
Page 29 of 43 Unreviewed manuscript
For Review Only
30
Jerina K, Krofel M, Stergar M, Videmšek U (2012) Factors affecting brown bear
685
habituation to humans: a GPS telemetry study. Final report. Biotechnical
686
Faculty, University of Ljubljana, Ljubljana, Slovenia.
687
Johnson HE, Breck SW, Baruch-Mordo S, Lewis DL, Lackey CW, Wilson KR,
688
Broderick J, Mao JS, Beckmann JP (2015) Shifting perceptions of risk and
689
reward: dynamic selection for human development by black bears in the
690
western United States. Biological Conservation 187: 164–172.
691
Kaczensky P, Knauer F, Krze B, Jonozovic M, Adamič M, Gossow H (2003)
692
The impact of high speed, high volume traffic axes on brown bears in Slovenia.
693
Biological Conservation 111: 191–204.
694
Kavčič I, Adamič M, Kaczensky P, Krofel M, Jerina K (2013) Supplemental
695
feeding with carrion is not reducing brown bear depredations on sheep in
696
Slovenia. Ursus 24: 111–119.
697
Kavčič I, Adamič M, Kaczensky P, Krofel M, Kobal M, Jerina K (2015) Fast food
698
bears: brown bear diet in a human-dominated landscape with intensive
699
supplemental feeding. Wildlife Biology 21: 1–8.
700
Kirby R, Macfarland DM, Pauli JN (2017) Consumption of intentional food
701
subsidies by a hunted carnivore. Journal of Wildlife Management.
702
Knight RR, Blanchard BM, Eberhardt LL (1988) Mortality patterns and
703
population sinks for Yellowstone grizzly bears, 1973–1985. Wildlife Society
704
Bulletin 16: 121–125.
705
Kokko H, Sutherland WJ (2001) Ecological traps in changing environments:
706
Ecological and evolutionary consequences of a behavioral mediated Allee
707
Page 30 of 43Unreviewed manuscript
For Review Only
31
effect. Evolutionary Ecology Research 3: 537–551.
708
Kristan WB (2003) The role of habitat selection behavior in population
709
dynamics: source-sink systems and ecological traps. Oikos 103: 457–468.
710
Krofel M, Dolšak K, Jerina K (2016) Optimizing dinner time in a risky restaurant:
711
Temporal segregation of brown bears at concentrated food sources. 24th IBA
712
International Conference on Bear Research & Management, At Anchorage,
713
Alaska, Anchorage, Alaska, USA.
714
Krofel M, Jerina K (2016) Mind the cat: Conservation management of a
715
protected dominant scavenger indirectly affects an endangered apex predator.
716
Biological Conservation 197: 40–46.
717
Krofel M, Jonozovič M, Jerina K (2012) Demography and mortality patterns of
718
removed brown bears in a heavily exploited population. Ursus 23: 91–103.
719
Laliberte A, Ripple W (2004) Range contractions of North American carnivores
720
and ungulates. BioScience 54: 123–138.
721
Lamb CT, Mowat G, McLellan BN, Nielsen SE, Boutin S (2017) Forbidden fruit:
722
human settlement and abundant fruit create an ecological trap for an apex
723
omnivore. Journal of Animal Ecology 86: 55–65.
724
Lamb CT, Mowat G, Reid A, Smit L, Proctor M, Mclellan BN, Nielsen SE, Boutin
725
S (2018) Effects of habitat quality and access management on the density of a
726
recovering grizzly bear population. Journal of Applied Ecology: 1–12.
727
Leclerc M, Frank SC, Zedrosser A, Swenson JE, Pelletier F (2017) Hunting
728
promotes spatial reorganization and sexually selected infanticide. Scientific
729
Page 31 of 43 Unreviewed manuscript
For Review Only
32
Reports 7: 45222.
730
Leclerc M, Vander Wal E, Zedrosser A, Swenson JE, Kindberg J, Pelletier F
731
(2016) Quantifying consistent individual differences in habitat selection.
732
Oecologia 180: 697–705.
733
Lesmerises R, St-Laurent M-H (2017) Not accounting for interindividual
734
variability can mask habitat selection patterns: a case study on black bears.
735
Oecologia 185: 415–425.
736
Loveridge AJ, Hamson G, Davidson Z, MacDonald DW (2009) African Lions on
737
the edge: reserve boundaries as “attractive sinks.” In: Macdonald DW,
738
Loveridge AJ (eds) Biology and Conservation of Wild Felids, 283–304. Oxford
739
University Press, Oxford.
740
Loveridge AJ, Searle AW, Murindagomo F, MacDonald DW (2007) The impact
741
of sport-hunting on the population dynamics of an African lion population in a
742
protected area. Biological Conservation 134: 548–558.
743
Loveridge AJ, Valeix M, Elliot NB, Macdonald DW (2017) The landscape of
744
anthropogenic mortality: how African lions respond to spatial variation in risk.
745
Journal of Applied Ecology 54: 815–825.
746
Mace RD, Waller JS, Manley TL, Lyon LJ, Zuring H (1996) Relationships
747
among grizzly bears, roads, and habitat use in the Swan Mountains, Montana.
748
Journal of Applied Ecology 33: 1395–1404.
749
Mattson DJ, Merrill T (2002) Expirations of grizzly bears in the contiguous
750
United States, 1850-2000. Conservation Biology 16: 1123–1136.
751
Page 32 of 43Unreviewed manuscript
For Review Only
33
Mazur R, Seher V (2008) Socially learned foraging behaviour in wild black
752
bears, Ursus americanus. Animal Behaviour 75: 1503–1508.
753
McLellan BN (2005) Sexually selected infanticide in grizzly bears: the effects of
754
hunting on cub survival. Ursus 16: 141–156.
755
McLellan BN (2015) Mechanisms underlying variation in vital rates of grizzly
756
bears on a multiple use landscape. Journal of Wildlife Management 79: 749–
757
765.
758
van der Meer E, Fritz H, Blinston P, Rasmussen GSA (2013) Ecological trap in
759
the buffer zone of a protected area: effects of indirect anthropogenic mortality
760
on the African wild dog Lycaon pictus. Oryx 48: 285–293.
761
van der Meer E, Rasmussen GSA, Fritz H (2015) Using an energetic cost–
762
benefit approach to identify ecological traps: the case of the African wild dog.
763
Animal Conservation: n/a-n/a.
764
Morehouse AT, Boyce MS (2017) Evaluation of intercept feeding to reduce
765
livestock depredation by grizzly bears. Ursus 28: 66–80.
766
Nellemann C, Støen OG, Kindberg J, Swenson JE, Vistnes I, Ericsson G et al.
767
(2007) Terrain use by an expanding brown bear population in relation to age,
768
recreational resorts and human settlements. Biological Conservation 138: 157–
769
165.
770
Nielsen S, Boyce M, Stenhouse G, Munro R (2002) Modeling grizzly bear
771
habitats in the yellowhead ecosystem of Alberta: taking autocorrelation
772
seriously. Ursus 13: 45–56.
773
Page 33 of 43 Unreviewed manuscript
For Review Only
34
Nielsen SE, Stenhouse GB, Boyce MS (2006) A habitat-based framework for
774
grizzly bear conservation in Alberta. Biological Conservation 130: 217–229.
775
Northrup JM, Pitt J, Muhly TB, Stenhouse GB, Musiani M, Boyce MS (2012a)
776
Vehicle traffic shapes grizzly bear behaviour on a multiple-use landscape.
777
Journal of Applied Ecology 49: 1159–1167.
778
Northrup JM, Stenhouse GB, Boyce MS (2012b) Agricultural lands as ecological
779
traps for grizzly bears. Animal Conservation 15: 369–377.
780
Ordiz A, Bischof R, Swenson JE (2013) Saving large carnivores, but losing the
781
apex predator? Biological Conservation 168: 128–133.
782
Ordiz A, Kindberg J, Sæbø S, Swenson JE, Støen OG (2014) Brown bear
783
circadian behavior reveals human environmental encroachment. Biological
784
Conservation 173: 1–9.
785
Ordiz A, Sæbø S, Kindberg J, Swenson JE, Støen OG (2017) Seasonality and
786
human disturbance alter brown bear activity patterns: implications for
787
circumpolar carnivore conservation? Animal Conservation 20: 51–60.
788
Ordiz A, Støen OG, Delibes M, Swenson JE (2011) Predators or prey? Spatio-
789
temporal discrimination of human-derived risk by brown bears. Oecologia 166:
790
59–67.
791
Ordiz A, Støen OG, Sæbø S, Kindberg J, Delibes M, Swenson JE (2012) Do
792
bears know they are being hunted? Biological Conservation 152: 21–28.
793
Oro D, Genovart M, Tavecchia G, Fowler MS, Martínez-Abrain A, In. (2013)
794
Ecological and evolutionary implications of food subsidies from humans.
795
Page 34 of 43Unreviewed manuscript
For Review Only
35
Ecology Letters 16: 1501–1514.
796
Palomero G, Ballesteros F, Nores C, Blanco JC, Herrero J, García-Serrano A
797
(2007) Trends in Number and Distribution of Brown Bear Females with Cubs-of-
798
the-year in the Cantabrian Mountains, Spain. Ursus 18: 145–157.
799
Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science
800
293: 1786–1790.
801
Patten MA, Kelly JF (2010) Habitat selection and the perceptual trap. Ecological
802
Applications 20: 2148–2156.
803
Penteriani V, Delgado MM, Melletti M (2010) Don’t feed the bears! Oryx 44:
804
169–170.
805
Penteriani V, Huber D, Jerina K, Krofel M, López-Bao J-V, Ordiz A, Zarzo-Arias
806
A, Dalerum F (in press) Trans-boundary and trans-regional management of a
807
large carnivore: Managing brown bears across national and regional borders in
808
Europe. Large carnivore conservation and management: Human dimensions
809
and governance.
810
Penteriani V, López-Bao JV, Bettega C, Dalerum F, Delgado M del M, Jerina K,
811
Kojola I, Krofel M, Ordiz A (2017) Consequences of brown bear viewing
812
tourism: A review. Biological Conservation 206: 169–180.
813
Pitman RT, Swanepoel LH, Hunter L, Slotow R, Balme GA (2015) The
814
importance of refugia, ecological traps and scale for large carnivore
815
management. Biodiversity and Conservation 24: 1975–1987.
816
Proctor MF, Paetkau D, McLellan BN, Stenhouse GB, Kendall KC, MacE RD et
817
Page 35 of 43 Unreviewed manuscript
For Review Only
36
al. (2012) Population fragmentation and inter-ecosystem movements of grizzly
818
bears in Western Canada and the Northern United States. Wildlife Monographs:
819
1–46.
820
Ripple WJA, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M et
821
al. (2014a) Status and ecological effects of the world’s largest carnivores.
822
Science 343: 1241484.
823
Ripple WJ, Estes J a, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M et
824
al. (2014b) Status and ecological effects of the world’s largest carnivores.
825
Science 343: 1241484.
826
Robbins CT, Schwartz CC, Felicetti LA (2004) Nutritional ecology of ursids: a
827
review of newer methods and management implications. Ursus 15: 161–171.
828
Robertson BA, Hutto RL (2006) A Framework for Understanding Ecological
829
Traps and an Evaluation of Existing Evidence. Ecology 87: 1075–1085.
830
Robertson BA, Rehage JS, Sih A (2013) Ecological novelty and the emergence
831
of evolutionary traps. Trends in Ecology and Evolution 28: 552–560.
832
Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary
833
traps. Trends in Ecology and Evolution 17: 474–480.
834
Schwartz C, Haroldson M, White G, Harris R, Cherry S, Keating K, Moody D,
835
Servheen C (2006) Temporal, Spatial, and Environmental Influences on the
836
Demographics of Grizzly Bears in the Greater Yellowstone Ecosystem. Wildlife
837
Monographs 161: 1–68.
838
Selva N, Teitelbaum CS, Sergiel A, Zwijacz-Kozica T, Zieba F, Bojarska K,
839
Page 36 of 43Unreviewed manuscript
For Review Only
37
Mueller T Supplementary ungulate feeding affects movement behavior of brown
840
bears. Basic and Applied Ecology.
841
Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to
842
human-induced rapid environmental change. Evolutionary Applications 4: 367–
843
387.
844
Sivertsen TR, Åhman B, Steyaert SMJG, Rönnegård L, Frank J, Segerström P,
845
Støen OG, Skarin A (2016) Reindeer habitat selection under the risk of brown
846
bear predation during calving season. Ecosphere 7: 1–17.
847
Skuban M, Finďo S, Kajba M, Koreň M, Chamers J, Antal V (2017) Effects of
848
roads on brown bear movements and mortality in Slovakia. European Journal of
849
Wildlife Research 63: 82.
850
Smith TS, Herrero S, DeBruyn TD (2005) Alaskan brown bears: habituation and
851
humans. Ursus 16: 1–10.
852
Steyaert SMJG, Kindberg J, Jerina K, Krofel M, Stergar M, Swenson JE,
853
Zedrosser A (2014) Behavioral correlates of supplementary feeding of wildlife:
854
can general conclusions be drawn? Basic and Applied Ecology 15: 669–676.
855
Steyaert SMJG, Kindberg J, Swenson JE, Zedrosser A (2013a) Male
856
reproductive strategy explains spatiotemporal segregation in brown bears.
857
Journal of Animal Ecology 82: 836–845.
858
Steyaert SMJG, Leclerc M, Pelletier F, Kindberg J, Brunberg S, Swenson JE,
859
Zedrosser A (2016a) Human shields mediate sexual conflict in a top predator.
860
Proceedings of the Royal Society B 283: 20160906.
861
Page 37 of 43 Unreviewed manuscript
For Review Only
38
Steyaert SMJG, Reusch C, Brunberg S, Swenson JE, Hackländer K, Zedrosser
862
A (2013b) Infanticide as a male reproductive strategy has a nutritive risk effect
863
in brown bears. Biology Letters 9: 20130624.
864
Steyaert SMJG, Zedrosser A, Elfström M, Ordiz A, Leclerc M, Frank SC et al.
865
(2016b) Ecological implications from spatial patterns in human-caused brown
866
bear mortality. Wildlife Biology 22: 144–152.
867
Støen OG, Ordiz A, Evans AL, Laske TG, Kindberg J, Fröbert O, Swenson JE,
868
Arnemo JM (2015) Physiological evidence for a human-induced landscape of
869
fear in brown bears (Ursus arctos). Physiology and Behavior 152: 244–248.
870
Stoner DC, Wolfe ML, Rieth WR, Bunnell KD, Durham SL, Stoner LL (2013) De
871
facto refugia, ecological traps and the biogeography of anthropogenic cougar
872
mortality in Utah. Diversity and Distributions 19: 1114–1124.
873
Stringham SF, Bryant A (2015) Distance-Dependent Effectiveness of
874
Diversionary Bear Bait Sites. Human-Wildlife Interactions 9: 229–235.
875
Swenson J, Sandegren F, Soderberg A, Bjarvall A, Franzen R, Wabakken P
876
(1997) Infanticide caused by hunting of male bears. Nature 386: 450–451.
877
Treves A, Krofel M, McManus J (2016) Predator control should not be a shot in
878
the dark. Frontiers in Ecology and the Environment 14: 380–388.
879
Trombulak SC, Frissel CA (2000) Review of ecological effects of roads on
880
terrestrial and aquatic communities. Conservation Biology 14: 18–30.
881
Vitousek PM, Mooney H a, Lubchenco J, Melillo JM (1997) Human Domination
882
of Earth’ s Ecosystems. Science 277: 494–499.
883
Page 38 of 43Unreviewed manuscript
For Review Only
39
Wielgus RB, Bunnell FL (2000) Possible negative effects of adult male mortality
884
on female grizzly bear reproduction. Biological Conservation 93: 145–154.
885
Wielgus RB, Bunnell FL, Wakkinen WL, Zager PE (1994) Population Dynamics
886
of Selkirk Mountain Grizzly Bears. The Journal of Wildlife Management 58: 266.
887
Wilson SM, Madel MJ, Mattson DJ, Graham JM, Burchfield JA, Belsky JM
888
(2005) Natural landscape features, human-related attractants, and conflict
889
hotspots: a spatial analysis of human-grizzly bear conflicts. Ursus 16: 117–129.
890
Wilson SM, Madel MJ, Mattson D. J, Graham JM, Merrill T (2006) Landscape
891
conditions predisposing grizzly bears to conflicts on private agricultural lands in
892
the western USA. Biological Conservation 130: 47–59.
893
Woodroffe R (2000) Predators and people: using human densities to interpret
894
declines of large carnivores. Animal Conservation 3: 165–173.
895
Zedrosser A, Steyaert SMJG, Gossow H, Swenson JE (2011) Brown bear
896
conservation and the ghost of persecution past. Biological Conservation 144:
897
2163–2170.
898
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Table legend
900
Table 1. The different scenarios that have been recognised as evolutionary or ecological traps for brown bears, as well as possible
901
trap scenarios and mechanisms that have the potential to affect the dynamics and viability of brown bear populations. For each trap
902
are detailed (a) the attractive resource triggering the trap, (b) the effects on bears (at both the individual and population levels), (c)
903
the bear class that may more easily fall into the trap and the expected severity of the demographic impact of the trap.
904
Trap Attractive resource Effects Attracted
individuals
Likely demographic
impacts
Human settlements Anthropogenic food Increased human caused mortality
Increased habituation to humans
Mainly young males Variable
Refuge from adult males Increased human caused mortality
Increased habituation to humans
Females with cubs Severe
Roads Food Increased human caused mortality Mainly young males Variable
Refuge from adult males Increased human caused mortality Females with cubs Severe
Artificial feeding sites Anthropogenic food Increased habituation to humans
Negative physiological impacts
Disruption of social stability
Variable Low
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Agricultural areas Food Increased human caused mortality Variable Variable
Reindeer husbandry Easy prey Increased human caused mortality Females with cubs Severe
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Figure legend
905
Figure 1. Graphical representation of evolutionary and ecological trap scenarios
906
and mechanisms that may affect brown bear populations in human-modified
907
landscapes. Traps occur when, because of human interference, the suitability of
908
high-quality habitats is decreased and/or settlement cues have been altered so
909
that the attractiveness of low-quality habitat is increased and unsuitable habitats
910
are preferred. This process may also affect the original properties and
911
attractiveness of source–sink systems. The habitat alterations provoked by
912
humans may cause brown bears to select relatively low-fitness options
913
(Behavioural mismatch), engender the emergence of traps resulting from either
914
increased preference for low-fitness options (Attraction), degraded fitness
915
opportunities without a concomitant decrease in preference (Degradation), or
916
both attraction and degradation simultaneously (Combination). To date, six
917
potential trap scenarios for brown bears have been detected in human-modified
918
landscapes: (1) important food resources close to human settlements; (2)
919
agricultural landscapes; (3) roads; (4) hunting for habitat selection cues of
920
females with cubs and young bears; (5) artificial feeding points and (6) other
921
leisure activities. Traps principally influence individual fitness and population
922
performance and viability. Depending on the quality of the trap habitat,
923
conservation efforts should mainly focus on improving the suitability of high-
924
quality traps or reducing the attractiveness of low-quality traps. This conceptual
925
framework is an elaboration of graphical representations from Sih et al. (2011),
926
Robertson et al. (2013) and van der Meer et al. (2015). (The brown bear photo
927
was downloaded from 123RF ROYALTY FREE STOCK PHOTOS,
928
http://www.123rf.com, Image ID 7119875, Eric Isselee).
929
Page 42 of 43Unreviewed manuscript
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Graphical representation of trap scenarios and mechanisms that may affect brown bear populations in
human-modified landscapes. Traps occur when, because of human interference, the suitability of high-
quality habitats is decreased and/or settlement cues have been altered so that the attractiveness of low-
quality habitat is increased and unsuitable habitats are preferred. This process may also affect the original
properties and attractiveness of source–sink systems. The habitat alterations provoked by humans
may cause brown bears to select relatively low-fitness options (Behavioural mismatch), engender the
emergence of traps resulting from either increased preference for low-
fitness options (Attraction), degraded
fitness opportunities without a concomitant decrease in preference (Degradation), or both attraction and
degradation simultaneously (Combination). To date, six (five demonstrated and one potential) trap
scenarios for brown bears have been detected in human-modified landscapes (see mai
n text): (1) important
food resources close to human settlements; (2) agricultural landscapes; (3) roads; (4) hunting for habitat
selection cues of females with cubs and young bears; (5) artificial feeding points and (6) other leisure
activities. Traps principally influence individual fitness and population performance and viability. Depending
on the quality of the trap habitat, conservation efforts should mainly focus on improving the suitability of
high-quality traps or reducing the attractiveness of low-quality traps. This conceptual framework is an
elaboration of graphical representations from Sih et al. (2011), Robertson et al. (2013) and van der Meer et
al. (2015). (The brown bear photo was downloaded from 123RF ROYALTY FREE STOCK PHOTOS,
http://www.123rf.com, Image ID 7119875, Eric Isselee).
254x190mm (96 x 96 DPI)
Page 43 of 43 Unreviewed manuscript
