Download Vigilance and food intake rate in paired and solitary Zenaida Doves

Ibis (2012), 154, 161–166
Short communication
Vigilance and food intake
rate in paired and solitary
Zenaida Doves Zenaida
aurita
1
FRANK CEZILLY, 1,2 * & ISMAEL KEDDAR 1
Université de Bourgogne, Equipe Ecologie Evolutive,
UMR CNRS 5561 Biogéosciences, 6 blvd. Gabriel,
21000 Dijon, France
2
Institut Universitaire de France
We quantified vigilance during feeding in the Zenaida
Dove Zenaida aurita, a tropical species with stable pairbonds and year-round territoriality. Both males and
females decreased the proportion of time spent vigilant
by 30% when feeding with their partner compared with
when feeding alone. This reduction was achieved
through increasing the length of inter-scan duration,
while scan duration remained constant. No evidence was
found for coordination of vigilance between pair members. The equal investment in vigilance by male and
female Zenaida Doves might be related to the mutual
benefits of long-term pair-bonding.
Keywords: foraging, monogamy, pair-bonding,
predation risk, scanning patterns.
Vigilance behaviour, defined as the interruption of an
activity to scan the environment, can serve multiple
functions, such as detection of predators or kleptoparasites (Lendrem 1983, Goss-Custard et al. 1999), monitoring of conspecifics for food (Robinette & Ha 2001),
and mate guarding and ⁄ or avoidance of unwanted copulations (Hario & Hollmen 2004). Consequently, levels of
vigilance may vary according to group size (Beauchamp
2008) as well as with the physiological state (Bachman
1993), social and ⁄ or reproductive status (Krams 1998,
Rieucau & Martin 2008) or age of individuals (Cézilly &
Boy 1988). In particular, sex-related differences in vigilance levels between pair members have been repeatedly
reported in socially monogamous bird species. Both in
monogamous galliforms (Dahlgren 1990, Artiss & Martin 1995) and in anseriforms (Sedinger & Raveling 1990,
*Corresponding author.
Email: [email protected]
ª 2011 The Authors
Ibis ª 2011 British Ornithologists’ Union
Gauthier & Tardif 1991, Forslund 1993, Gauthier-Clerc
et al. 1998, Christensen 2000, Quan et al. 2003, Squires
et al. 2007), higher levels of vigilance in males occur
primarily to protect females and chicks from predators,
enabling them to devote more time to feeding and, secondly, to prevent extra-pair copulations. The opposite
pattern has been observed in White-breasted Nuthatches
Sitta carolinensis, in which females are more vigilant than
males when feeding in pairs, presumably to avoid kleptoparasitic attacks from their partners (Waite 1987).
So far, however, all quantitative studies of vigilance
behaviour in socially monogamous birds have been conducted in species living in temperate areas, characterized
by seasonal reproduction and intermittent pair-bonding.
By contrast, little is known about the vigilance behaviour
of socially monogamous bird species living in the tropics.
The behavioural ecology of tropical monogamous bird
species differs from that of temperate species (Mock
1985, Stutchbury & Morton 2001, 2008, Macedo et al.
2008), especially in the maintenance of year-round territoriality and extended pair-bonds (Freed 1987, Stutchbury & Morton 2001). One supposed benefit of extended
pair-bonds is shared vigilance, resulting in decreased predation risk and increased food intake (McKinney 1986).
In addition, the maintenance of extended pair-bonds may
favour cooperation between mates in various tasks (Bossema & Benus 1985, St-Pierre et al. 2009), including
anti-predatory vigilance (Black 2001). Coordination in
vigilance might be easier to achieve in pairs than in larger
groups (Ferrière et al. 1996, 1999, Rodríguez-Gironés &
Vásquez 2002, Fernández-Juricic et al. 2004).
We studied vigilance behaviour in a tropical monogamous bird, the Zenaida Dove Zenaida aurita, a species
with long-term pair-bonding and high mate fidelity (F.
Cézilly unpubl. data), on the island of Barbados (West
Indies). There, Zenaida Doves have colonized the urban
habitat and are very tolerant of humans, making their
study and observation particularly easy (Lefebvre 1996).
Zenaida Doves typically defend their territories yearround, alone or in pairs, although in some areas they may
form large feeding aggregations where food is particularly
abundant (Sol et al. 2005, Monceau et al. 2011). Pairs
usually maintain close proximity while foraging, with no
aggression between males and females, unlike the pattern
often observed in seasonally breeding monogamous bird
species (Waite 1987, Steer & Burns 2008, Menzies &
Burns 2010). Zenaida Doves are largely granivorous birds
(Wiley 1991), although in urbanized habitat they also
exploit food scraps left by humans. While foraging on
the ground, they regularly raise their heads briefly to scan
the environment, as observed in several other dove
species (Greig-Smith 1981, Cézilly & Brun 1989, Dias
2006). Although natural predators, including raptors, are
absent from Barbados, introduced predators such as
domestic cats and mongooses Herpestes javanicus regularly prey upon Zenaida Doves (F. Cézilly unpubl. data).
162
F. Cezilly & I. Keddar
M E T HO D S
Study population
Fieldwork took place from early February to mid-March
2010 at two sites, the Sunset Crest area and the Folkestone Park, both situated near Holetown (1310¢60¢¢N,
5938¢60¢¢W). The Sunset Crest area covers about
0.6 km2, and consists of about 300 private villas with
gardens, a few parks, and some commercial buildings
and parking areas. The Folkestone Park covers about
0.03 km2, and includes the St-James’ Church, its adjacent cemetery, the Folkestone recreational area and a
beach. The study benefited from the presence of a ringed
population of Zenaida Doves of known sex (through the
use of molecular sexing methods), with each individual
wearing a unique combination of coloured plastic rings,
allowing individual identification at distance (Monceau
et al. 2011).
Recording vigilance behaviour
Vigilance behaviour was recorded during feeding using a
Sony HDR-FX 1000E High Definition video camera.
Video sequences were recorded at 25 frames per second
with a 1 ⁄ 10 000 second shutter speed to obtain highresolution video footage. All video recordings were made
between 06:30 and 12:00 h and between 14:00 and
16:00 h. Only weak variation in light intensity occurred
between recordings because the sky was bright with very
little cloud cover, and overcast sky conditions occur
infrequently in Barbados during the February–March
period (Haraksingh 2001). Furthermore, a recent study
(Blackwell et al. 2009) indicated that variation in light
intensity has little effect on the ability to visually detect
an approaching object in the closely related Mourning
Dove Zenaida macroura.
To control for food quality and density (Beauchamp
2009), a bowl feeder, measuring 12 cm in diameter and
containing 140 g of a standard mix of millet, sorghum
and oat seeds (Roberts Cage and Aviary Bird Feed;
Roberts Manufacturing, St Michael, Barbados), was used
(Fig. 1). The large quantity of seeds ensured that no
Figure 1. A ringed pair of Zenaida Doves feeding at a bowl
feeder. The male (on the left) is feeding while the female (on
the right) is vigilant. Note the eye partly covered by the eyelids
in the male.
ª 2011 The Authors
Ibis ª 2011 British Ornithologists’ Union
food depletion would occur during the course of recordings. The feeder was always at a distance of at least 5 m
from any cover to control for the potential confounding
effect of distance to cover (Poysa 1994, Slotow & Rothstein 1995). The camera was placed 5 m from the
feeder, and the observer 10 m behind the camera. Preliminary experiments indicated that at such a distance,
the behaviour of the birds was not altered by human
presence. Video recording was triggered when an individual started to feed, using a Sony RM-VD1 wired
remote control, and lasted up to 10 min. The ambient
sound around the feeder was simultaneously recorded
while filming so as later to distinguish routine vigilance
(sensu Blanchard & Fritz 2007) from scans induced in
reaction to sharp auditory stimuli, such as human voices,
car horns or alarm calls from other bird species, such as
Carib Grackles Quiscalus lugubris (see Griffin et al.
2005).
Both single and paired individuals were videorecorded. The mating status of birds was determined
prior to video-recordings through regular observations at
the two study sites in 2010 and, in some cases, from previous observations of the same pairs in the preceding
years. For each pair that was filmed, we also attempted
to record the vigilance behaviour of each pair member
when feeding alone, in the absence of its partner. The
time between two video-recordings of the same individual varied between 1 and 3 days.
Analysing vigilance behaviour
Contrary to a previous study on another dove species
(Cézilly & Brun 1989), preliminary observations did not
reveal any difference in the morphology of head movements during scanning in Zenaida Doves. We therefore
restricted our analyses to continuous bouts of undisturbed routine vigilance, excluding bouts with scans
induced in reaction to the auditory perturbations that
we could identify. Vigilance sequences were analysed
frame by frame for 2 min (corresponding to 3000 frames
analysed for each individual). During the analysis of
video-recordings, the observer (I.K.) was blind to the sex
of individuals. Analysis started at the beginning of a state
(scan or inter-scan) and stopped at the end of the state
in which the individual was at the 3000th frame. For
each of the sequences, the number of frames for which
an individual was scanning the environment (i.e. vigilant,
with head up) and the number of frames for which the
individual was feeding (i.e. non-vigilant, with head
down) were counted. Hence, for each bird, the proportion of time spent vigilant, as well as the duration of
each scan and each inter-scan interval were obtained. In
most video-recordings, the food intake rate (expressed as
seeds consumed per minute) could be determined from
the quantification of the swallowing movements of the
birds.
Vigilance and food intake rate in Zenaida Doves
Statistical analysis
All statistical analyses were conducted using the R
software (R Development Core Team 2008). Both the
proportion of time spent vigilant and the food intake
rate were arcsin square-root transformed to obtain a
better fit to the normal distribution. Durations of both
scan bouts and inter-scan bouts did not fit any known
distribution, even after transformation. Hence, parametric tests (Sokal & Rohlf 1995) were used to analyse
both the proportion of time spent vigilant and food
intake, whereas non-parametric tests (Siegel & Castellan
1988) were used to compare scan duration and the
duration of inter-scan intervals. A regression model was
used to test for the effect of the proportion of time
spent vigilant by one member of a pair upon the food
intake rate of its partner. The effects of sex and social
context (i.e. feeding alone or in the presence of the
partner) on the proportion of time spent vigilant and
on the food intake rate were investigated using linear
mixed-effect models, with pair as a random factor
(Pinheiro & Bates 2000).
Coordination of vigilance between pair members was
investigated by comparing the observed proportion of
time when both pair members were scanning and that
expected under the assumption of random and independent scanning by the two individuals. This expected proportion is the product of the proportion of time spent
vigilant by the male of the pair and the proportion of
time spent vigilant by the female of the pair. Normality
was achieved through a logit transformation, and proportions were compared with a paired t-test.
163
R ES ULT S
We obtained recordings of males and females feeding
together for 12 pairs of ringed birds, of which 18 individuals (eight males and 10 females) were also filmed
while foraging in the absence of their partner. We were
able to quantify food intake rate in paired birds when
feeding in the presence of their partner in 11 of 12 pairs,
and when feeding alone in eight males and nine females.
In addition, we obtained recordings for seven single
males and five single females feeding alone and could
quantify food intake in all birds except one female.
Vigilance patterns did not differ between males and
females in single individuals (permutation test for two
independent samples: proportion of time spent vigilant,
P = 0.168; scan duration, P = 0.481; inter-scan interval
duration, P = 0.116; nm = 7, nf = 5), or in paired individuals when feeding alone (proportion of time spent vigilant, t16 = 0.651, P = 0.524; scan duration, Mann–
Whitney test, W = 43.5, nm = 8, nf = 10, P = 0.779;
inter-scan interval duration, W = 33, P = 0.563). Overall, vigilance patterns did not differ between single individuals (n = 12) and paired ones feeding alone (n = 18;
proportion of time spent vigilant, t28 = 0.229,
P = 0.820; scan duration, Mann–Whitney test,
W = 131.5, P = 0.308; inter-scan duration, W = 95.5,
P = 0.611).
Within paired birds, the proportion of time spent vigilant was significantly influenced by the social context
(F1,14 = 27.739, P = 0.0001), but not by sex
(F1,7 = 0.678, P = 0.438) or the interaction between sex
and social context (F1,14 = 1.720, P = 0.211; Fig. 2a).
Reduction in vigilance while feeding in a pair was
Figure 2. (a) Mean proportion of time spent vigilant by Zenaida Doves (back-transformed data) according to sex (males: white bars,
females: grey bars) and social context. Vertical bars show standard deviations. (b) Mean food intake rates of Zenaida Doves
(back-transformed data) according to sex (males: white bars, females: grey bars) and social context. Vertical bars show standard
deviations.
ª 2011 The Authors
Ibis ª 2011 British Ornithologists’ Union
164
F. Cezilly & I. Keddar
achieved through an increase in inter-scan duration
(Wilcoxon signed rank-test, V = 12, n = 18, P = 0.001;
data pooled for males and females), whereas scan duration did not differ according to social context (Wilcoxon
signed rank-test, V = 29, n = 18, P = 0.452, after correction for ties; data pooled for males and females), and sex
had no influence on either variable (inter-scan duration,
V = 27.5, n = 12, P = 1; scan duration, V = 32, n = 12,
P = 0.965, after correction for ties). Social context had a
significant and positive influence on food intake rate
(F1,12 = 10.930, P = 0.006), whereas neither sex
(F1,6 = 0.257, P = 0.631) nor the interaction between
sex and social context (F1,12 = 0.164, P = 0.693) influenced food intake (Fig. 2b). The proportion of time
spent vigilant by the partner had no significant effect on
the rate of food intake in either females (regression
analysis, R2 = 0.089, n = 12, P = 0.372) or males
(R2 = 0.0002, n = 12, P = 0.965).
There was no evidence for coordination of vigilance
patterns between mates, as the observed proportion of
time spent with at least one pair member scanning the
environment was actually 11% higher than the random
expectation based on independent scanning by the two
partners (paired t-test, t11 = 4.460, P = 0.001).
DI S CU SS IO N
Foraging in a pair led to a reduction of about 30% in the
proportion of time spent vigilant by Zenaida Doves compared with when foraging alone, with no significant difference between males and females. This reduction was
due to an increase in the length of inter-scan intervals,
whereas scan duration did not vary significantly whether
birds foraged alone or in a pair. Obviously, the provision
of clumped and easily accessible food in our experiments
made searching effort unnecessary, thus potentially altering the relative payoffs of foraging and vigilance. However, a detailed study of feeding and vigilance in another
dove species (Cézilly & Brun 1989) has shown that the
influence of social context on vigilance was independent
of whether the food was clumped or not.
The absence of a sex-related difference in vigilance
contrasts with previous studies of socially monogamous
bird species observed in temperate areas (Waite 1987,
Dahlgren 1990, Artiss & Martin 1995, Guillemain et al.
2003, Quan et al. 2003, Squires et al. 2007). From a
mechanistic point of view, equal levels of vigilance in
males and females, when foraging both alone or in a pair,
might be linked to the absence of elevated levels of
androgens in males of tropical bird species. Indeed,
androgen levels are typically low in males of tropical bird
species compared with males of bird species living in
temperate areas, and particularly so in species with
long-term pair-bonds and year-round territorial defence
(Goymann et al. 2004, Hau et al. 2008), such as Zenaida
Doves. Interestingly, Fusani et al. (1997) have shown
ª 2011 The Authors
Ibis ª 2011 British Ornithologists’ Union
that male vigilance is positively related to androgen
levels in the Grey Partridge Perdrix perdrix, where males
are typically more vigilant than females during the
breeding season (Dahlgren 1990). It would therefore be
valuable to compare sex-related differences in vigilance
behaviour between tropical monogamous bird species
with various lengths of reproductive season and monogamous bird species living in temperate areas, to assess
whether the pattern observed in the present study has
some generality. Alternatively, the lack of difference in
vigilance behaviour between the sexes might be due to a
change in female behaviour, under the form of increased
vigilance in response to high predation risk.
From an adaptive point of view, equal levels of vigilance between sexes might be related to the low level of
sexual selection acting on Zenaida Doves. Several studies
reporting higher levels of vigilance in males of socially
monogamous bird species have been conducted just
prior to egg-laying, at the time of peak female fertility
(Gauthier & Tardif 1991, Artiss & Martin 1995, Christensen 2000, Squires et al. 2007). In such circumstances,
male vigilance may not only act to detect predators, but
may also be a form of mate guarding. In addition, higher
vigilance in males is often observed in sexually dimorphic species, where males are markedly larger and ⁄ or
more colourful than females (Bertram 1992, Guillemain
et al. 2003, Squires et al. 2007). In contrast, Zenaida
Doves can make breeding attempts at any time of year,
although a peak in reproduction is observed from January to May (Wiley 1991). The species shows little sexual
dimorphism in size, with males being on average only
5% larger than females (Dechaume-Moncharmont et al.
2011), and there is no obvious difference in coloration
between sexes. In addition, recent evidence (Quinard
2010) indicates that both territorial males and females
react to territorial intrusions by conspecifics irrespective
of the sex of the intruder, suggesting that mate guarding
is not intense in this species.
Finally, it has been suggested that coordination of vigilance is favoured when animals have a low probability
of detecting an approaching predator with their head
down, and a high probability of being warned when
another member of the group detects a danger (Fernández-Juricic et al. 2004, see also Bednekoff 2001). These
two conditions are fulfilled in the Zenaida Dove. First, in
both pigeons and doves, the eyes are partly closed while
pecking at food, with the eyelids forming a slit that
leaves a part of the pupil uncovered (Fig. 1). Partial
shutting of the eyelids increases the focal depth of retinal
images at extreme near-field viewing-conditions, thus
facilitating pecking at food, while reducing visual acuity
at distance-viewing conditions (Ostheim 1996, 1997) at
the expense of the ability to detect an approaching predator. Secondly, Zenaida Doves react instantaneously to
the acoustic whistles associated with the wing beats of
their partners as they ascend from the ground when
Vigilance and food intake rate in Zenaida Doves
startled (Coleman 2008, F. Cézilly pers. obs.) However,
despite very favourable conditions a priori, we found no
evidence for coordination in vigilance between pair
members in Zenaida Doves. The amount of time with
no partner being vigilant was actually above the random
expectation based on the assumption of independent
scanning by the male and the female of a pair when
feeding together. One possibility is that this temporal
overlap in scanning resulted from pair-members occasionally reacting simultaneously to some distant visual
stimuli that we failed to identify during the image analysis of video recordings.
Our results show that the pattern of vigilance in pairs
of a tropical monogamous bird species differs from that
previously observed in species living in temperate areas.
The more equal investment in vigilance by male and
female Zenaida Doves when feeding in pairs may be
related to the mutual benefit of long-term pair-bonding.
One important question that remains open, however, is
whether the benefits of reduced vigilance and increased
food intake translate into differential survival between
paired and unpaired birds. Long-term monitoring of
banded individuals may help to assess the benefits of
year-round pair-bonded monogamous species living in
tropical environments.
We are particularly grateful to Mr Steve Devonish, Director of
Natural Heritage (division of Ministry of Environment and
Drainage of Barbados) and Kim Downes Agard for granting us
the permission to capture and ring Zenaida Doves. We thank
Laurine Belin for help in recording and analysing patterns of vigilance in Zenaida Doves during the initial stage of the project,
and Nicole Atherley, Laurent Brucy, Christine Dubreuil, Karine
Monceau, Sébastien Motreuil and George Prato for help in
catching, banding and sexing birds. The study was supported by
the Agence Nationale pour la Recherche (programme blanc
Monogamix), and the Centre National de la Recherche Scientifique.
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Received 2 March 2011;
revision accepted 23 August 2011.
Associate Editor: Ian Hartley.