Download Scanning pattern of greater rheas, Rhea americana

J Ethol (2009) 27:429–436
DOI 10.1007/s10164-008-0137-5
ARTICLE
Scanning pattern of greater rheas, Rhea americana: collective
vigilance would increase the probability of detecting a predator
Mariana E. Carro Æ Gustavo J. Fernández
Received: 23 June 2008 / Accepted: 29 October 2008 / Published online: 5 December 2008
Ó Japan Ethological Society and Springer 2008
Abstract Many models using vigilance to predict the
probability of detecting an approaching predator assumes
that prey scanning events should be produced at random.
Consequently, the length of intervals among successive
scans must follow a negative exponential distribution. We
analyzed the scanning behavior of the greater rhea, Rhea
americana, which is a gregarious, flightless bird, in eastern
Argentina. We investigated whether individual and/or
collective scanning departed from random and whether this
departure varied with group size. We used two simulation
models based on observed scanning sequences to assess the
effectiveness of vigilance on the individual and collective
level when faced with an opportunistic or stalking predator.
The analysis of 59 behavioral sequences of wild greater
rheas foraging solitary or in groups of two to six or more
individuals revealed that the inter-scan length of individual
sequences significantly departed from random. In contrast,
inter-scan intervals for collective vigilance were shorter
than individual ones, but only fit the random expectation
for groups of two and five individuals. Models showed that
collective vigilance could increase the probability of
detecting a predator, thereby reducing their vulnerability,
independent of whether the predator uses a stalking or
opportunistic approaching strategy.
M. E. Carro (&) G. J. Fernández
Laboratorio de Ecologı́a y Comportamiento Animal,
Departamento de Ecologı́a, Genética y Evolución,
Facultad de Ciencias Exactas y Naturales,
Universidad de Buenos Aires, Int Guiraldes s/n, Pabellón II,
Ciudad Universitaria, C1428EHA Buenos Aires, Argentina
e-mail: [email protected]
Keywords Collective vigilance Group size Individual vigilance Instantaneous randomness Predation risk Rhea americana
Introduction
Vigilance is one of the main behavioral mechanisms that
many prey use to avoid being depredated. Such behavior
allows individuals to detect an approaching predator early
and then escape from it (Elgar 1989; Caro 2005). However,
scanning for predators usually precludes animals from
performing other activities, such as foraging, thereby
highlighting the compromise between reducing vulnerability through vigilance and using the time on other vital
activities (Lind and Cresswell 2005).
Several studies have shown that individual vigilance
could decrease with increasing group size, assuming that
individuals benefit from living in groups through both
dilution and detection effects (see Bertram 1980; Pulliam
and Caraco 1984; Lima and Dill 1990 for reviews). The
reduction of vigilance by individuals in groups is presumably counterbalanced by an increased collective
detection probability (i.e. the probability that any individual of the group detects an approaching predator; Pulliam
1973). Several researchers who have carried out observational and experimental studies agree that large groups
would benefit from this collective vigilance (e.g. observational studies: Caraco 1979; Elgar and Catterall 1981;
Jarman 1987; Ebensperger et al. 2006; experimental studies: Lima 1995; Boland 2003).
Studies have shown that for the greater rhea (Rhea
americana), which is a large, flightless and gregarious bird,
individual vigilance decreases with increasing group size
(Martella et al. 1995; Reboreda and Fernández 1997).
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However, Fernández et al. (2003) found that this decrease
did not affect the collective vigilance, which remained
unchanged and independent of group size. This result
apparently implies that in addition to the increased time
available for foraging when one individual was in a group,
collective vigilance would not improve the probability of
detecting an approaching predator. However, the detection
of predators depends not only on the time spent in vigilance
but also on the manner in which vigilant events are produced (Roberts 1994; Scannell et al. 2001). Therefore, in
this study, we analyzed the scanning pattern of greater
rheas during solitary foraging or foraging in groups of two
to six or more individuals.
Original models using vigilance to predict the detection
probability of an approaching predator assume that prey
scanning events are produced at random (Pulliam 1973).
Although random scanning was initially assumed in order
to simplify the mathematical model (Bednekoff and Lima
1998), it was subsequently assumed to be biologically
relevant as it might reduce the chance of an effective
predator attack based on the unpredictability of the scanning events (Bednekoff and Lima 2002). According to this
hypothesis, the predator is unable to predict when the prey
will scan and, therefore, cannot effectively time its attack.
Furthermore, following a random scanning event, the frequency distribution of inter-scan interval lengths must
follow a negative exponential distribution (i.e. instantaneous randomness; Bednekoff and Lima 1998). This
vigilance pattern has been revealed for ostriches (Struthio
camelus), house sparrows (Passer domesticus) and blue tits
(Parus caerulescens) (Bertram 1980; Elcavage and Caraco
1983; Lendrem 1983, respectively), but other studies have
failed to show this pattern (Lendrem 1984; Sullivan 1985).
In the latter studies, birds seem to avoid very short and very
long inter-scan intervals. It has been suggested that long
inter-scan intervals might be used by predators in timing
their attacks and passing undetected by the prey (Lendrem
et al. 1986). On the other hand, the use of short inter-scan
intervals reduces the time available for other useful activities, such as feeding. Moreover, the information that is
acquired by the prey from closely timed scans about the
risk of predation is unlikely to yield new information over
short periods of time. Furthermore, predators need a minimum amount of time to reach the detection threshold
distance beyond which the prey is unable to escape.
Therefore, scanning more frequently than the approaching
speed of predators would be a waste of time for prey.
A number of authors have recently suggested that prey
may cope with the increased risk of predation by using a
regular vigilance pattern (Scannell et al. 2001; Bednekoff
and Lima 2002). Although a regular scanning pattern is
more predictable due to a reduction in the variance of interscan interval lengths, it offers the prey maximum efficiency
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in detecting the attack of an opportunistic, non-stalking
predator (Bednekoff and Lima 2002). It also offers an
alternative explanation for a scanning pattern that differs
from the expected random pattern. However, Scannell
et al. (2001) suggested that a random scanning pattern
could still be advantageous when prey face a predator that
adapts its attacking behavior to the scanning pattern of the
prey.
In the study reported here we specifically investigated
whether individual and collective rhea scanning patterns
depart from instantaneous randomness and if this departure
varies with group size. If scanning events occur in a random manner, the distribution of inter-scan lengths should
follow a negative exponential distribution (Hart and
Lendrem 1984). Finally, we assessed whether observed
collective scanning patterns would improve the probability
of detecting a theoretical predator attack as compared to
individual vigilance patterns; to this end, we used two
simple simulation models that consider a predator using a
stalking or an opportunistic (i.e. non-stalking) strategy.
Materials and methods
Study species
Greater rheas are large (about 20–24 kg), gregarious birds
that inhabit most of South America. This large bird forages
for grasses and insects in open habitats, usually in groups
of 2–20 or more individuals; however, it occasionally can
be found as a solitary bird (Hudson 1920; Bruning 1974).
Males are slightly larger than females and have black
plumage at the crown and the base of the neck. Rheas feed
themselves by walking over the terrain, with their heads
about 50 cm from the ground approximately 76% of the
time (Carro and Fernández 2008); this feeding behavior is
interrupted when they lift their heads to look around. The
large open areas in which this species was studied offer no
cover for retreat when an approaching predator poses a
threat.
Field methods and data collection
We analyzed the behavioral sequential data of 59 observations of the wild greater rheas at General Lavalle,
Province of Buenos Aires, Argentina (36°250 S, 56°560 W)
during the 1995, 1996 and 1999 non-breeding seasons
(April–August) and at Ayacucho (37°090 S 58°290 W) during the 2005 non-breeding season. These sites contain
highly homogeneous pastures that are mainly grazed by
cattle. No natural predators of adult rheas (i.e. cougar, Felis
concolor) are currently present in the region, but rheas are
hunted by feral dogs and, on occasion, by humans.
J Ethol (2009) 27:429–436
Rhea groups were video-recorded with a Sony Hi8
camcorder (Sony Corporation, Tokyo, Japan) from inside a
vehicle at distances of100–200 m in an effort to minimize
any disturbances from our presence. We avoided filming
groups where individuals were clearly disturbed by our
presence, as evidenced by the group or individual animals
moving away from us and exhibiting unusually long scan
periods. The groups consisted of 1–12 adult greater rheas
that were foraging usually less than 50 m away one from
one another. Group membership could change as individuals were allowed to leave the group and join the group
freely, but changes in group membership rarely occurred
during our observations because groups were usually more
than 300 m away from one another. When one individual
moved away from the group for more than 50 m, we
stopped the register. Since the birds were not marked and
moved freely within the study area, we possibly made
repeated observations of the same bird in some cases, but
the chance of this occurring was rare because we went
through the study area in a systematic manner. Moreover, if
we recorded a bird more than once, it was on a different
date or at a different place. The video-recording started
15–20 min after we arrived at the birds’ foraging area. Data
were collected from 0730 to 1930 h, and the group
recording lasted up to 10–15 min or when the focal animal
moved out of sight. The average length of the recordings
was 483.35 s ± 133.08 [mean ± standard deviation (SD);
n = 59; range 206.1–671.9 s].
Data analysis
Animal behavior was registered from videotapes using an
event recorder program (Etholog 2.5.5). We used the focal
sampling method to obtain individual behavioral sequences
and the all-animal sampling method to obtain the collective
behavioral sequences (Lehner 1998). We defined two
behavioral categories: vigilance and inter-scan—and considered these categories to be mutually exclusive. We
defined vigilance as the bird stretching its neck upwards
while looking around, either still in one spot or moving
among the foraging sites (see Reboreda and Fernández
1997). Inter-scan behaviors included any others behaviors
that were displayed by the focal animal (preening, walking
and feeding). Feeding and vigilance account for about
80–90% of the greater rhea’s daily activities (Reboreda and
Fernández 1997). For the purposes of this study, we did not
include any birds that displayed, were the target of
aggressive or courtship behaviors or remained resting during the video-recording. We pooled the data for groups of
6–12 adults due to the low numbers of these groups. On
each register, we noted the temporal sequence of events and
the length of each event. We estimated the proportion of
time that was spent by individuals on vigilance, the median
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length of the vigilant events and the scanning rate for each
individual. The scanning rate was estimated as the number
of vigilant events divided by the total length of observation.
Collective vigilance was measured as the proportion of
time that at least one individual of the group remained
vigilant. Inter-scan intervals were then estimated as the
time that remained among successive vigilant events by
any individual within the group.
The data are presented as mean ± standard error (SE).
We used parametric tests when possible; otherwise, we
used equivalent non-parametric tests.
Instantaneous randomness analysis
We used a generalized distribution function, the gamma
distribution, to assess whether the distribution of inter-scan
lengths fit a negative exponential distribution. The gamma
distribution is a generalization of the exponential distribution, but it is more flexible in its shape characteristics
and tractable for statistical inference (Matis et al. 1992).
This distribution is characterized by the following two
parameters: a is the shape parameter that determines the
shape of the curve, and b represents the scale parameter,
which describes the location of the curve and is an estimator of the mean value of the variable when the variable
follows an exponential distribution. Note that when a = 1,
the gamma distribution represents an exponential distribution, whereas when a [ 40, the gamma distribution
approaches a normal distribution. We fit the observed
distribution of inter-scan intervals with the expected
intervals according to a gamma distribution with a = 1 and
assessed the fit using Kolmogorov–Smirnov tests. Since
this test is sensitive to small samples, we pooled individual
data from birds that were in groups of the same size. We
also used a gamma distribution to fit the observed interscan data and to estimate parameters a and b for the distribution of inter-scan behaviors of each group size. Again,
fitting was tested by the Kolmogorov–Smirnov statistic.
Variations of a and b with the group size were assessed
using simple regression analyses.
We also evaluated whether the length of inter-scan
intervals could be predicted from the mean length of
intervals (Kramer and Bell 1996). We estimated the mean,
the variance and the coefficient of variation (CV) of interscan lengths for all sequences in order to test whether
predictability varied with the group size. Mean values were
estimated as the product between a and b, whereas variance was estimated as the product between a and b2
(Mermoz and Garcı́a 2006). Kramer and Bell (1996) suggested that a low CV for inter-scan intervals would reflect a
regular scanning pattern and thus a higher predictability.
Inter-scans for collective vigilance were assessed in a
similar manner as that used for individual values. In this
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case, inter-scan intervals involved the time period where no
individual was vigilant. We pooled data for groups of the
same size and estimated parameters a and b by fitting the
observed inter-scans to a gamma distribution. We also
fitted the observed distribution of inter-scan intervals to a
gamma distribution with a = 1 (exponential distribution).
We estimated the mean, the variance, and the CV for interscan lengths for all sequences in order to assess their variation as associated with group size. Mean length and CV
for the length of the inter-scan intervals as estimated from
the gamma distribution were compared with those obtained
from individual sequences for animals in groups of the
same size.
Probability of predator detection
We used two simple simulation models based on observed
scan–inter-scan sequences to assess whether the observed
variation in the scanning patterns affect the probability of
detecting a theoretical attack. Firstly, we considered a
predator that does not synchronize its attacks with the
behavior of the prey—i.e. it attacks its prey in a random
fashion—which implies that it is an opportunistic predator.
Then, over each individual and collective scan sequence,
we simulated ten attacks by selecting randomly generated
time values from the beginning of the vigilance sequences
to when the predator launches its attack. For collective
vigilance, perfect detection was assumed. The attack was
composed based on the time that the predator takes to
approach to the minimum distance threshold d (the
detection threshold; Lima 1987; Bednekoff and Lima
2002) for which the prey could not escape even if it
detects the approaching predator. This approaching time
was represented by s, and in successive simulations,
arbitrary values of 2, 5, 10, and 15 s were used. Typically,
the approaching time s depends on the predator’s speed
and the efficiency of the prey’s response (Bednekoff and
Lima 2002). Unfortunately, data regarding the approaching speed for actual predators in our study area are
unavailable. However, by considering other predators,
such as dogs, which have an approaching speed of
approximately 40 km/h, we choose values to represent the
approaching distances that range from 20 m (s = 2 s) to
160 m (s = 15 s). For each sequence, we estimated the
relative risk rs as the proportion of attack events in which
the simulated predator was successful in its attack over the
total number of simulations (n = 10). An attack was then
considered to be successful (S = 1) when td C s, where td
is the difference in time between the time at which the
predator launches the attack and the time that the prey
initiates the next scanning event; attacks were considered
to be unsuccessful when td \ s. Then, rs is the proportion
of successful attacks.
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The second model assumes a stalking predator that
synchronizes its attacks with the prey’s inattentive periods.
Relative risk rs is
Pn
ðti sÞ
for ti s;
rs ¼ i¼1
Tt
where ti is the length of the inter-scan interval i, and Tt is
the total time that an individual (or group) remained inattentive (i.e. the sum of all inter-scan intervals). For ti B s,
rs is equal to zero. In this case, the relative risk of being
depredated is a function of the distribution of inter-scan
intervals of individuals or groups. We compared individual
and collective sequences of the proportion of events where
the theoretical predator was able to approach without being
detected between groups and different approaching times
using two-way analysis of variances (ANOVAs). The data
were transformed using the arcsine of the square root of the
value to meet the requirements of the statistical parametric
tests.
Results
The proportion of time that was spent in vigilance for
individual rheas decreased with increasing group size
(Kruskal–Wallis test v2 = 13.56, df = 5, P = 0.02;
Fig. 1a). Accordingly, the individual scanning rate
decreased with increasing group size, but the length of each
scan event remained constant and independent of the
number of individuals within the group (Kruskal–Wallis
tests v2 = 13.43, df = 5, P = 0.02; v2 = 1.58, df = 5,
P = 0.90, respectively; Fig. 1b, c). No sexual differences
were detected as related to the proportion of time spent in
vigilance, the length of vigilant events or the scanning rate
(Mann–Whitney tests N# = 43, N$ = 16; Z = -1.94,
P = 0.06, Z = -0.89, P = 0.37, Z = -1.57, P = 0.18,
respectively). Then, in a posteriori analysis, we pooled the
observations corresponding to males and females.
Collective vigilance did not vary with the group size
(Kruskal–Wallis test, v2 = 8.94, df = 5, P = 0.11). The
mean proportion of time that a group was vigilant was
0.18 ± 0.10 (mean ± standard deviation).
Instantaneous randomness
The frequency distribution of inter-scan lengths of individual sequences departed significantly from those expected
according to an exponential distribution for all group sizes
(Kolmogorov–Smirnov tests P \ 0.05). The mean shape
parameter (a) for observed inter-scan intervals was 1.50,
which is a slightly higher value than expected when
following an exponential distribution (i.e. a = 1). For
individual sequences of vigilance, the scale parameter (b)
J Ethol (2009) 27:429–436
70
a
60
0.14
Interval length (seg)
Proportion of time spent vigilant
0.16
433
0.12
0.10
0.08
Individual
Collective
50
40
30
20
0.06
10
0.04
0
1
0.02
2
3
4
5
6 or more
Group size
0.060
b
Fig. 2 Mean and SE values of inter-scan intervals for individual
(filled circle) and collective (open circle) vigilance sequences of
greater rheas in groups of two to six or more individuals
Scanning rate (bouts / s)
0.055
0.050
0.045
0.040
0.035
0.030
0.025
0.020
0.015
3.2
c
Median scan length (s)
3.0
2.8
2.6
2.4
2.2
2.0
1.8
1.6
1.4
1
2
3
4
5
6 or more
Group size
Fig. 1 Proportion of time that an individual remained vigilant (a),
individual scanning rate (b) and median length of scans (c) of greater
rheas (Rhea americana) foraging in groups of one to six or more
individuals. Mean ± standard error (SE) are represented
tended to increase with the group size, although this relationship was not significant (regression analysis
F1,4 = 9.26, P = 0.06). Individuals in larger groups scan
less often, thereby increasing the length of inter-scan
intervals. The shape parameter (a) remained constant across
different group sizes (Regression analysis F1,4 = 0.52,
P = 0.51).
For collective vigilance, the distribution of inter-scan
intervals departed from the expectation of randomness for
groups of three, four and six or more individuals (Kolmogorov–Smirnov tests P \ 0.05) but not for groups of
two and five individuals (Kolmogorov–Smirnov tests
P [ 0.05). The mean shape parameter (a) for observed
inter-scan intervals was 1.38, which is a value lower than
the estimated value for individual sequences but also
slightly higher than expected for a negative exponential
distribution (i.e. a = 1). Both the scale (b) and shape (a)
parameters did not vary with group size (regression analyses F1,4 = 0.75, P = 0.44, and F1,4 = 0.73, P = 0.44).
The mean length of the inter-scan intervals for collective
vigilance was lower than that for the individual vigilance
for groups of two to six or more birds (Welch’s approximate t-tests for means P \ 0.05 for all groups). The CVs of
inter-scan intervals were similar for individual and collective vigilance sequences (Z-test P \ 0.05 for all groups).
The mean CVs were 0.82 ± 0.05 (±standard deviation)
and 0.85 ± 0.05 (±standard deviation) for individual and
collective sequences, respectively. Therefore, collective
vigilance sequences presented shorter inter-scan intervals
and lower variance than individual ones (Fig. 2).
Probability of predator detection
When detection depends on individual vigilance, the relative risk of being preyed by an either an opportunistic
or stalking predator increases with increasing group size
but decreases with increasing s (F5.84 = 6.83, P \ 0.001;
F3.84 = 29.99, P \ 0.001, respectively, for an opportunistic predator; F5.84 = 11.95, P \ 0.001; F3.84 = 146.12;
P \ 0.001, for a stalking predator; Fig. 3a, b).
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J Ethol (2009) 27:429–436
Proportion of successful events
1.0
}
a
0.8
τ =2
0.6
τ =15
0.4
0.2
0.0
Proportion of successful events
1.0
b
0.8
0.6
0.4
}
τ =2
}
τ =15
0.2
0.0
1
2
3
4
5
6 or more
Group size
Fig. 3 Mean and SE proportion of successfully simulated predation
events according to the observed individual (solid lines) and
collective (dashed lines) vigilance sequences of greater rheas in
different group sizes. Model assumes that the probability of the
predator detection is based on the individual vigilance (filled symbols)
and on the collective vigilance (open symbols). a Simulations
assuming that the predator starts its attack randomly (i.e. at any time
and independently of the prey’s behavior), b simulations assuming
that the predator starts its attack synchronizing it with inattentive
periods of the prey. We show only the results of simulations that
consider the detection threshold (s) equal to 2 and 15 s. For collective
vigilance, perfect detection was assumed
When birds used the information from other group
members (i.e. collective vigilance), the risk of being depredated decreased with increasing group size and s for both
an opportunistic and a stalking predator (F5.74 = 13.59,
P \ 0.001; F3.74 = 45.22; P \ 0.001, F5.74 = 8.29,
P \ 0.001; F3.74 = 78.28; P \ 0.001 for an opportunistic
and stalking predator, respectively; Fig. 3a, b).
Discussion
Previous studies have shown that greater rheas reduce their
individual vigilance as group size increases (Martella et al.
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1995; Reboreda and Fernández 1997) but that collective
vigilance remains unchanged (Fernández et al. 2003).
Although this pattern appears to imply that the effectiveness of vigilance does not vary with the group size, the
detection of approaching predators may depend on the
distribution of the vigilance events (Roberts 1994; Scannell
et al. 2001). Traditionally, researchers have suggested that
the most effective vigilance pattern is one that consists of
randomly produced scanning events. Although such randomly produced scans were initially assumed in vigilance
models solely for the purpose of mathematical simplicity
(Bednekoff and Lima 1998), they may still offer the prey a
major benefit due to the reduction in the predictability of
scans, thereby reducing the chance of a predator timing its
attack during a period of prey inattentiveness (Bednekoff
and Lima 2002).
Our studies on individual inter-scan duration in greater
rhea vigilance sequences also revealed a significant,
although slight, departure from the expectation of randomness mainly due to the avoidance of short inter-scan
intervals. Individuals in large groups used longer inter-scan
intervals, which caused a reduction in the vigilance rate and
an increase in the variance of the duration of these intervals.
This variation in the scanning pattern was also found in
earlier studies in which birds used longer inter-scan intervals
as group size increased, also indicating a marked departure
from the expectation of random vigilance (e.g. Bertram
1980; Sullivan 1985; Cresswell 1994; Beauchamp 2006).
All of these characteristics are unfavorable for prey in large
groups and contrary to the expected benefits of living in
groups. Individuals in large groups then take major risks
relative to those in smaller groups or solitary birds by
adopting longer inattentive inter-scan intervals, which ultimately may favor the synchronization of a predator attack.
Rheas showed a pattern of collective vigilance different
from that of individual vigilance. The length of the interscan intervals was shorter than those observed in the
individual vigilance sequences and remained independent
of the group size. These shorter inter-scan intervals could
thereby reduce the probability of being surprised by an
attacking predator. Although inter-scan intervals for collective vigilance departed from a random pattern, unlike
the individual vigilance, they exhibited a more regular
scanning pattern because the variance of the inter-scan
intervals in collective vigilance was lower than that in
individual vigilance, and it did not vary with group size.
Researchers have recently proposed that regular scanning
patterns could be advantageous for prey that face randomly
attacking predators, such as raptors or canids (Scannell
et al. 2001; Bednekoff and Lima 2002). In addition to the
reduction of the length of scans, regularity in the scanning
pattern could facilitate the rheas’ ability to detect a predator attack (Bednekoff and Lima 2002).
J Ethol (2009) 27:429–436
All of these findings appear to support the idea that
greater rheas benefit from living in groups. Simulations
provided additional evidence that supports this hypothesis.
When we considered the collective scanning sequences, the
probability of detecting a predator attack increased when
the prey faced both an opportunistic and stalking predator.
Although the efficiency for group detection of an
approaching predator depends on the efficiency of the
information that is gathered among the group members
(Treherne and Foster 1981), the reduction in this efficiency
could be similar to a reduction in the time that predators
take to approach to the prey (s). In our simulations, the risk
of a predator remaining undetected increased when we
reduced s, but the animals still appeared to benefit from
grouping. Lower values of s are probably the least realistic
in biological terms because they indicate the attack of a
predator that is very close to the prey or which has a high
attack speed. More realistic biological values would be
higher, implying longer approaching times for the predator
and a higher probability of detection for the prey.
Collective detection has been recognized as being more
typical of small groups of birds or mammals because
individual behavioral changes that follow the detection of a
predator are more readily distinguishable from other nonpredator driven behavioral responses (Lima 1995). In a
related species, the emu, Dromaius novaehollandiae,
Boland (2003) showed that individuals in large groups
detect an approaching predator (e.g. human) sooner than
individuals in smaller groups. In our studied population of
greater rheas, group sizes rarely surpassed 20 individuals
(typical group size = 7.6 individuals; Carro and Fernández
2008). Additionally, our study population of greater rheas
usually moved in small groups that may have facilitated
collective detection. Escape movements in greater rheas
involve a rapid fleeing run in an evasive zigzag path that
can reach a speed of approximately 40 km/h. This is
clearly different from the slow walk that these animals
exhibit while foraging. We also found that disturbances
usually generated a rapid response in all group members,
which included increasing their attentiveness and eventually provoking the escape response.
In addition to the benefit that is provided by collective
vigilance in terms of increased safety provided by the
cooperative vigilance within the group, extra benefits arise
from staying in large groups as the probability of an individual of being preyed upon decreases with increasing
group size (i.e. ‘‘dilution effect’’; Dehn 1990). However,
larger groups are not always safer. The benefits of the
dilution effect in large groups are reduced if predators
preferentially prey upon a subset of group members
(Treves 2000). Despite the fact that we did not incorporate
the dilution benefit in our analyses, it presumably remains
present in the rhea groups that we analyzed as they
435
correspond to groups formed only by adults, and we do not
have evidence to suggest that predators differentially hunt
males or females. Moreover, we provided additional evidence that greater rheas may obtain benefits from the
collective detection of potential predators.
In this study, we may also have underestimated the
detection efficiency of the greater rhea. We assumed that
vigilance and other behaviors were mutually exclusive
activities. However, it has been suggested that foraging
animals that have their head down can still gather information from the context of their situation. In this case,
vigilance would not be restricted only to a head-up posture
(Lima and Bednekoff 1999; Cresswell et al. 2003;
Fernández-Juricic et al. 2004). Although this could be true
for greater rheas foraging in pastures, like those where we
performed this study, animals with higher scanning rates
and upright postures would have an improved probability
of detecting an approaching predator.
Although the results reported here do not indisputably
prove the real ability of rheas foraging in groups to detect a
predator, we propose that the reduced collective inter-scan
intervals provide individuals with improved chances of
detecting a predator. Collective vigilance can compensate
for a reduction in the vigilance behavior of the individual
as predicted by the ‘‘many eyes’’ hypothesis (Pulliam
1973). Therefore, our results appear to support the
hypothesis that group-living for rheas would be favored by
the decreased predation risk. Earlier studies on other large
and gregarious ratites that inhabit open habitats found that
these species also benefit from group living (Bertram 1980;
Boland 2003). We would therefore expect that group-living
increases in those species as predation risk increases.
Caraco et al. (1980) found that in the yellow-eyed junco
(Junco phaeonotus), the individuals gravitated towards
greater groups as the frequency of predator attacks
increased. Particularly in rheas, if collective detection is an
effective approach to reducing the predation risk, as we
have proposed, groups in habitats where native predators
still remain should be larger than those we found in our
study area. Further studies should focus on examining this
prediction and also on the efficiency of group vigilance in
this species in terms of the detection and escape from an
approaching predator to test the predictions derived from
this study.
Acknowledgments We thank V. Simoy and F. Milano for logistical
support and field assistance at Ayacucho. M. Beade and M. Mermoz
provided GJF with field assistance at General Lavalle. We thank
J. Boote, R. Paso and A. Guzman for allowing us to perform the study
on their cattle ranches. We also thank C. Battagliese for checking the
English grammar and M. Mermoz and two anonymous reviewers for
their comments on an earlier version of this MS. This study
was supported by a grant of University of Buenos Aires to GJF
(Programación UBACYT 2004–2007 X007).
123
436
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