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Weietal. BMC Ecol (2020) 20:41
https://doi.org/10.1186/s12898-020-00309-3
RESEARCH ARTICLE
Risk assessment intheplateau pika
(Ochotona curzoniae): intensity ofbehavioral
response diers withpredator species
Wanrong Wei1,2*, Qiaoyan Zhen3, Zhongmin Tang4 and Maria K. Oosthuizen5,6
Abstract
Background: The ability of a prey species to assess the risk that a predator poses can have important fitness advan-
tages for the prey species. To better understand predator–prey interactions, more species need to be observed to
determine how prey behavioral responses differ in intensity when approached by different types of predators. The
plateau pika (Ochotona curzoniae) is preyed upon by all predators occurring in its distribution area. Therefore, it is an
ideal species to study anti-predator behavior. In this study, we investigated the intensity of anti-predator behavior
of pikas in response to visual cues by using four predator species models in Maqu County on the eastern Qinghai-
Tibetan Plateau.
Results: The behavioral response metrics, such as Flight Initiation Distance (FID), the hiding time and the percentage
of vigilance were significantly different when exposed to a Tibetan fox, a wolf, a Saker falcon and a large-billed crow,
respectively. Pikas showed a stronger response to Saker falcons compared to any of the other predators.
Conclusions: Our results showed that pikas alter their behavioral (such as FID, the hiding time and the vigilance)
response intensity to optimally balance the benefits when exposed to different taxidermy predator species mod-
els. We conclude that pikas are able to assess their actual risk of predation and show a threat-sensitive behavioral
response.
Keywords: Predator–prey interactions, Plateau pika, Anti-predator behavior, FID, The hiding time, Vigilance
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Background
It is crucial for prey species to evaluate and respond
adaptively to risks posed by their predators, as predators
have strong direct and indirect risk effects on prey spe-
cies. Prey species can be exposed to a wide range of pred-
ator species that differ in size [1], density [2], habitat use
[3], diel activity [4] and hunting styles [5] in natural sys-
tems. Studying the behavioral response intensity of prey
to risks posed by different predator species, is therefore
an important component of improving our understand-
ing of predator–prey interactions [6, 7].
Predation is a pervasive selection force that influences
physiological, morphological, and behavioral adapta-
tions in prey species in order to increase the chances
of a successful escape [8]. Generally, the assessment of
predation risk is translated into the display of an anti-
predator behavior. Antipredator behavioral responses to
predation risks include a reduction in foraging activity
[9, 10], increased vigilance [11, 12], reduced movement
[13], reduced use of conspicuous behavioral displays [14],
increased hiding time in a refuge or shelter [14, 15], and
increased alarm calls [16, 17]. However, these behavio-
ral strategies have associated costs, as they can provoke
a reduction in factors such as energy intake, energetic
Open Access
BMC Ecology
*Correspondence: weiwr18@126.com
1 Key Laboratory of Southwest China Wildlife Resources Conservation,
College of life Sciences, China West Normal University, Nanchong 637009,
China
Full list of author information is available at the end of the article
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Weietal. BMC Ecol (2020) 20:41
investment in defensive structures, or lower mating suc-
cess. As risk assessment is difficult to quantify, most
studies use Flight Initiation Distance (FID), the hiding
time in a refuge and vigilance as the metrics to study
the risk levels associated with antipredator behaviors of
prey species [7, 14, 18–22]. FID is the distance at which
a prey starts to flee upon approach of a predator [23,
24]. Prey approached by predators often flee into refuges
and emerge after a brief stay [15, 25]. e hiding time is
the time from the moment that prey hides in refuge to
the moment that it re-emerges again [26]. Vigilance is
the time that prey spend in gathering information that
is used to observe predators and assessing the potential
predation risk [27]. In general, a longer FID, a longer
hiding time in a refuge and higher vigilance means that
the prey is experiencing a higher risk of predation [22,
26–33].
A growing number of studies demonstrated that prey
can assess their actual risk of predation and shape their
antipredator effort accordingly in response to different
degrees of predation threat, which supports the threat-
sensitive predator avoidance hypothesis. e threat-sen-
sitive predator avoidance hypothesis has been verified in
many animals, including insects, crabs, fish, amphibians,
reptiles, mammals and birds [23, 28, 34–40]. ese stud-
ies have shown that prey usually exhibit different anti-
predator behavioral response intensities when attacked
by predator species which exhibit different levels of pre-
dation risks. However, to our knowledge, this hypothesis
has rarely been tested in small, burrowing, grassland her-
bivores in the wild.
e plateau pika (Ochotona curzoniae) is a small, diur-
nal, social burrowing herbivorous lagomorph, which
occurs in most areas above an altitude of 3300 m in
the Tibetan plateau [41]. e pika is an ideal species to
study the assessment of predation risk because they are
preyed upon by nearly all of the predators occurring on
the plateau. ese predators include wolves (Canis lupis),
Tibetan foxes (Vulpes ferrilata), snow leopards (Uncia
uncia), brown bears (Ursus arctos),steppepolecat(Mus-
telaeversmanni), Alpine weasel (Mustela altaica pal-
las), golden eagles (Aquila chrysaetos), upland buzzards
(Buteo hemilasius), saker falcons (Falco cherrug), gos-
hawks (Accipiter gentilis), black kites (Milvus migrans),
little owls (Athene noctua) and large-billed crows (Corvus
macrorhynchos tibetosinensis) [42–44]. Previous studies
demonstrated that the Tibetan fox and the Saker falcon
are regarded as the most threatening predators for pikas
since the Tibetan fox is a pika specialist [45, 46] and pikas
are a main food source of the Saker falcon (90% of pellets
under the nest of a Saker falcon contained pika remains)
[42]. Wolves and crows hunt pikas opportunistically or
when other food is scarce, but generally do not pose a
serious risk to pikas [7, 47, 48]. In addition, a previous
study found that pikas responded differently when they
were presented with the calls of different predators [7].
erefore, it is believed that different types of predators
represent different risk levels to pikas [7].
Encounters between predator and prey are rarely
observed in nature. For this reason, the predator models
have been evaluated using indirect studies [49–53]. In this
study, we conducted a field experiment to test ‘the threat-
sensitive predator avoidance hypothesis’ using burrow-
ing plateau pikas. We exposed the pikas to four of their
common predators, the Tibetan fox, wolf (Canis lupis),
Saker falcon and large-billed crow, representing different
levels of predation risk to the pikas. We assumed that the
Tibetan fox and Saker falcon are more threatening preda-
tor species than the wolf and large-billed crow based on
whether pikas are the main food source for these preda-
tors. We hypothesized that the pika would have the abil-
ity to assess the level of predation risk and exert different
behavior response intensities when exposed to different
predator species models. Specifically, we predicted that:
(1) pikas would be longer FID when exposed to a more
threatening predator species model; (2) the hiding time
in a refuge would be longer after an unsuccessful ‘attack’
by a more threatening predator species model; and (3)
pikas would allocate more time to vigilance (vigilance is
defined as the total duration of time that a pika has its
head lifted above its back) when they re-emerge from a
refuge after an unsuccessful ‘attack’ by a more threaten-
ing predator species model.
Results
When approached by a saker falcon, crow, fox or wolf,
pikas maintained 16.8m, 7.1m, 8.8m and 5.1m in FID,
respectively (Fig.1a, b; Fig.2). Pikas spent 898s, 263s,
299s and 248s in the refuge, respectively, following
an unsuccessful predation by a saker falcon, crow, fox
or wolf (Fig.1a, b; Fig.2). In addition, when reemerg-
ing from the refuge, pikas spent about 74%, 57%, 61%
and 56% of their time during the first 10min on vigi-
lance after an unsuccessful predation by a saker fal-
con, crow, fox or wolf, respectively (Fig.1a, b; Fig.2). A
mixed linear model analysis showed that SM (F = 7.492,
p = 0.001) and GS (F = 34.864, p < 0.001) had signifi-
cant effects for FID, while P (F = 0.058, p = 0.944) and
EO (F = 0.907, p = 0.533) had not, and the interaction
effects between SM and GS was significant (F = 6.187,
p = 0.002). However, for the hiding time in the refuge,
Kruskal–Wallis tests showed a significant difference
across different predator species model treatments
(p < 0.05). After the p was adjusted, we found no signifi-
cant difference between wolf and crow (p = 1; Fig . 2),
fox and crow (p = 0.163; Fig. 2) and between saker
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Page 3 of 8
Weietal. BMC Ecol (2020) 20:41
falcon and fox (p = 0.120; Fig.2). However, there was a
significant difference between wolf and fox (p = 0.004;
Fig. 2), between wolf and saker falcon (p < 0.001;
Fig.2) and between crow and saker falcon (p < 0.001;
Fig. 2). A mixed linear model analysis showed that
SM (F-value = 6.329, p = 0.002) and GS (F = 16.684,
p < 0.001) had significant effects in vigilance, while P
(F = 0.780, p = 0.468) and EO (F = 1.288, p = 0.285)
had not. However, the interaction effects (F = 3.573,
p = 0.026) of SM and GS did differ significantly in
vigilance.
Discussion
e results from our study provide evidence that pikas
display different behavioral response intensities when
exposed to different predator species models. e saker
falcon is perceived as the greatest threat by pikas as it
elicited the strongest anti-predator behavioral response,
with the longest FID and hiding time in the refuge, and
the highest vigilance percentage. Our results support the
‘threat-sensitive predation avoidance hypothesis’ that
pikas have the ability to assess the degree of risk posed
by a predator, and that responses are graded in intensity
depending on the threat level perceived [49, 54]. Com-
pared to the previously studies [7, 48], this is the first
report to assess pika anti-predator behavior in response
to the presence of different predator species. ese
results provide valuable information that may be used in
the biological control of one species that can be inhibited
by using the interrelationships with another species.
Prey minimizes the cost of escape by remaining where
they are until the potential cost of staying outweighs
the benefits [19, 21, 55]. is suggests that when a prey
detects a predator early, it should delay escape attempts
until some criterion relating to escape costs to the cost
of not fleeing is met. According to the escape theory,
Fig. 1 The flight initiation distance (a) and the vigilance time (b) of
pika response to the models of four of their native predators (wolf,
fox, crow and saker falcon). Data presented are means with standard
errors
Fig. 2 The hiding time of pika response to the models of four of their
native predators (wolf, fox, crow and saker falcon). Data presented
are means with standard errors. Significant difference (based on a
non-parametric multiple test at alpha < 0.05) is denoted by pairs of
lower case letters
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Weietal. BMC Ecol (2020) 20:41
predators with a higher risk are associated with greater
FID [56, 57], while FID is expected to be shorter when
predation risk is lower [58]. Our results showed that the
FID was strongly influenced by the SM. GS is known to
affect the ability of prey animals to detect predators [59],
which then alter the FID [38]. We also found GS has a
significant influence on FID.
Prey often respond to predator attacks by hiding in
their refuges or safe microhabitats [60, 61]. However,
remaining in refuges can also incur fitness costs, and
the decision of when to come out from a refuge after an
unsuccessful attack by a predator is an important compo-
nent of anti-predator behavior [21, 22]. ere is a trade-
off between staying in refuge with a diminishing risk of
predation over time, but with the increased risk of star-
vation while in the refuge [10, 61, 62]. Cooper and Fred-
erick [21] demonstrated that the hiding time in a refuge
should be longer when the perceived risk is higher. Our
results are similar to previous studies [24, 63, 64], and
support the view that the hiding time in refuge changed
with exposure to different predators which present differ-
ent level of risk.
e level of vigilance is associated with predation
risk and vigilance can increase the ability of prey to
gather information about the current predation risk [7,
9]. In addition, the vigilance level of prey depends on
the level of previous predation risk [9]. In general, prey
reduced foraging time and engaged in anti-predator
behavior when the previous predation risk was high [9].
Our results indicate that the vigilance level was signifi-
cantly higher in response to a saker falcon compared to
the other predators, which indicates pikas perceive the
saker falcon as the greatest risk of our four test predator
species.
Aerobic movements of animals is energetically costly,
especially in QTP [41]. e reduction of unneces-
sary aerobic movements lowers energetic costs and
can increase the survival rate of pikas [41]. Pikas have
adapted to display varying anti-predator behavioural
response intensities depending on the level of risk
posed by different predators [7]. e results of the pre-
sent study indicate that the saker falcon is regarded as
the most dangerous predator because pikas elicited
the strongest anti-predator response (for example, the
furthest FID, the longest hiding time in refuge and
the highest vigilance percentage) when exposed to it.
A possible explanation for the difference in responses
elicited by the different predators is the difference in
the approach speed of the different predator species.
Zhang etal. [7] suggested that raptors (eagle and fal-
con) are more threatening than beasts (fox and wolf)
because raptors approach faster. In contrast, our results
indicate that the threat of a fox is greater than that of
a crow [7]. us, a more likely explanation for the dif-
ference in behavioral response intensities are related
to whether the pika is the main food resource for the
specific predator. In addition, our results also indicate
that the saker falcon poses a greater threat to pikas
than the fox, implying that pikas are able to evaluate
risk levels by assessing the predator visually and having
stronger antipredator behavioral responses when facing
a more threatening predator. e ability to discriminate
between more and less dangerous predators can have
significant advantages for pika survival. Many other
animals also vary their behavioral response intensity
depending on the predator species [23, 28, 34–40], and
this adaptation is as a result of co-evolution with preda-
tors over millions of years [7]. However, it is not known
whether the ability of pika to discriminate between
predators is innate or based on experience and would
require further studies to elucidate this.
Predators play an important role in the control of
pikas as the direct and indirect predation risk effects
can significantly affect the fertility and survival of
pikas [45, 65]. Over the past decades, plateau pikas
have been targeted for control by poisoning primarily
because they are believed to have a negative impact on
rangeland and compete with livestock for food [43]. An
unfortunate consequence of these poisoning campaigns
to kill pikas is that the predator species may inadvert-
ently be poisoned [43]. Besides that, many predators of
pikas are being killed for profits [48]. e situation is
further exasperated by the fact that the pika fertility is
far greater than that of its predators [48], and the pika
population can recover rapidly to its original state in a
short time [66]. whereas the predator numbers remain
low due to the killing and poisoning campaigns. Essen-
tially the natural mechanism of pika population control
is eliminated from the system, and the pika populations
continue to increase unchecked. erefore, it is impera-
tive that the poisoning campaigns and the killing of car-
nivore campaigns should be halted.
Conclusions
Our results show that pikas are able to discriminate
between predator species which present different lev-
els of risk and alter their response according to what is
likely to be a larger threat. In addition, our results also
provide support to previous studies suggesting that the
saker falcon is the most threatening predator of pikas in
the alpine meadow of the Qinghai-Tibet Plateau. Finally,
given the critically important role of predators of pikas
in controlling their population densities we urge that the
campaigns to poison pikas and the killing of their carni-
vore predators should be terminated.
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Weietal. BMC Ecol (2020) 20:41
Materials andmethods
Study site
e study site is located in a natural alpine meadow in
Luqu County, Gansu province, northwestern China.
Geographically, the study site is located on eastern part
of Qinghai-Tibetan plateau (lat. 34° 14′ N; long. 102° 13′
E; alt. 3650m). e site has a typical alpine continental
climate, with mean annual temperatures of 2.3°C. e
average annual precipitation is 543.6 mm, and occurs
predominantly between June and September. e main
soil type is subalpine meadow soil. e vegetation type is
alpine meadow, and dominant species is Kobresia humi-
lis, Elymus nutans, Festuca ovina L, Polygonum vivipa-
rum L, Anemone obtusiloba D. e inclination of study
site (plateau pika habitat) is about 13° on a western slope.
In this area, the distribution of pika families is patchy
and each family contains 4–7 individuals. In our study
area, the range of the active area of a pika family is about
470–680m2.
Experiment design
e experiments were conducted 15–29 June, 2016,
after the breeding season. We randomly selected three
different pika populations (P) which were spatially non-
adjacently distributed in our study site. Ten days before
the start of the experiment, we placed two iron pillars
(50cm diameter, 3m high) in each area, where one pil-
lar was situated in the pika colony, the other was situ-
ated on the slope above the pika habitat, and the distance
between the two pillars was 50m (Fig.3). e two pil-
lars were connected by a rope that was strong enough
to hold and slide the predator models. e height of the
rope was adjusted depending on the predator species.
We fixed an infrared high definition camera (Huian: WL-
1008T, LED, 2megapixel, 12.8, Progressive ScanCMOS,
1920 × 1080fps) that can rotate 360° on the pillar that
was in the colony, and used a cable to connect it to a
computer (Lenovo, G5050) in a tent that was 400 m
away from the pika colony. During the experiments, the
anti-predator behavior of the pikas were observed and
recorded. We tested four different conditions: a wolf
(length: 135cm, width: 25cm, height: 30cm), a Tibetan
fox (length: 50cm, width: 15cm, height: 35cm), a large-
billed crow (length: 10cm, width: 5cm, height: 15 cm)
and a saker falcon (length: 45cm, width: 150cm, height:
25cm). e four predator models served as the predator
species models (SM) (Fig.4). Each population was tested
for 4 cycles (each cycle was 2days long) and the interval
between cycles was at least 2days. A cycle consisted of
presenting each of the four predators to a colony of pikas.
e order (EO) of the predators was randomized to avoid
habituation of the pikas to the experimental procedure,
while the interval between different predators in a cycle
was at least 3h. In addition, we recorded the survey dates
(SD) of SM in different P.
During the experimental procedures, the predator
models were placed on the rope and a person dragged the
model from the upper pole to the lower pole inside the
pika colony with a rope by walking 80m away (Human
activities affect the activity of pikas at distances closer
than 30m) [66], parallel to the model at a speed of 5m/s.
When pikas hid in their burrows, the predator model was
moved back up to the upper pole. Tests were conducted
in the morning during peak hours of pika activity (8:00–
9:00) on a sunny day. Taking into account the height of
the animal and its hunting style, we adjusted the height
to 40cm, 90cm, 120cm and 130cm for the tibetan fox,
wolf, large-billed crow and Saker falcon, respectively. Tri-
als were stopped if there were predators in the surround-
ing environments.
We analyzed the videos at one quarter speed and
scored the hiding time and vigilance using J Watcher
1.5.0. In our experiments, we only observed adult pikas
whose vigilance direction was opposite to that of the
approaching predator model to determine the FID
because vigilance direction can influence the FID [23,
67]. In addition, group size (GS) was quantified as it can
also influence FID [7]. When all experiments were ana-
lyzed, we measured the FID and the refuge distance (RD)
measured for individual observed pikas, the FID and
refuge distance was measured to the nearest 0.1m. e
hiding time was defined as the period between first adult
retreating, to the first adult pika emerging again from
burrows [7]. Finally, we measured the vigilance percent-
age within ten minutes once the pika has left the burrow
entrance. e vigilance is the total duration of time that a
pika has its head lifted above its back, regardless whether
it was quadrupedal or bipedal [68].
Fig. 3 The Sample selection and the black wireframe is the active
area of pikas. The range of active area of a pika family is about
470–680 m2 in our study area
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Weietal. BMC Ecol (2020) 20:41
Data analyses
To improve normality, the FID was reciprocally trans-
formed and vigilance was square root transformed, and
were tested with general linear models in SPSS 22.0.
Pearson correlation coefficients were used to identify
collinearity among independent variables. To control
for multicollinearity, we tested correlations of pairs of
independent variables. Association between variables
was assessed using the Spearman correlation index (Rs)
and was considered significant when p < 0.05. We only
maintain one of the correlated collinear variables in the
next analysis. e effect of SM on the FID was analyzed
using a mixed linear model with GS and RD as covari-
ates, P and SD and EO as random variables and SM as
a fixed variable, RD and SD were not included as pre-
dictors in the LMMs as GS and RD, SD and EO were
highly collinear. en we fit a model without RD and
SD to test for the main effects. e effect of SM on the
vigilance was analyzed using a mixed linear model with
GS as covariates, P and SD and EO as random varia-
bles and SM as a fixed variable, SD was not included
as a predictor in the LMMs as SD and EO were highly
collinear. en we fit a model without SD to test for
the main effects. All interactions among these were
included in the model and removed if not significant.
However, hiding time was not normally distributed
despite multiple transformations, therefore we used
Nonparametric Tests (Kruskal–Wallis) followed by all
pairwise multiple comparisons.
Abbreviations
FID: Flight initiation distance; P: Pika populations; SM: Species models; EO:
Order; SD: Survey dates; GS: Group size.
Acknowledgements
We thank Shenghui An for assistance with the field work.
Authors’ contributions
WRW and QYZ designed the study and analysed the data, WRW, ZMT and
QYZ carried out the fieldwork, WRW drafted the manuscript, MKO revised the
manuscript, which was commented by all co-authors. All authors gave final
approval for publication. All authors read and approved the final manuscript.
Funding
This research was financially supported by the Special Fund for Agro-Scientific
Research in the Public Interest (201203041), the Fundamental Research Funds
of China West Normal University (18Q046), and the Gansu Provincial Science
and Technology Program (1054nkcp159).
Availability of data and materials
The datasets used and analysed during the current study are available from
the corresponding author on reasonable request.
Ethics approval and consent to participate
All fieldwork was carried out according to the national legislation. The behav-
ioral studies were in compliance with the legal regulations of China and were
approved by the Laboratory Animal Ethics Committee of China West Normal
University.
Fig. 4 Four different taxidermy predator species models: a Tibetan fox (Vulpes ferrilata). b Wolf (Canis lupis). c Saker falcon (Falco cherrug). d
Large-billed Crow (Corvus macrorhynchos)
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Weietal. BMC Ecol (2020) 20:41
Consent to publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Author details
1 Key Laboratory of Southwest China Wildlife Resources Conservation, College
of life Sciences, China West Normal University, Nanchong 637009, China.
2 State Key Laboratory of Grassland Agro-Ecosystems, College of Pastoral Agri-
culture Science and Technology, Lanzhou University, Lanzhou 730200, China.
3 China West Normal University, Nanchong 637009, China. 4 Gannan Grassland
Workstation in Gansu Province, Hezuo 747000, China. 5 Department of Zool-
ogy and Entomology, University of Pretoria, Private Bag X20, Hatfield 0028,
South Africa. 6 Mammal Research Institute, University of Pretoria, Hatfield 0028,
South Africa.
Received: 25 June 2019 Accepted: 13 July 2020
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