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Bird Study
ISSN: 0006-3657 (Print) 1944-6705 (Online) Journal homepage: http://www.tandfonline.com/loi/tbis20
Co-occurrence and commensal feeding between
Little Egrets Egretta garzetta and Eurasian
Spoonbills Platalea leucorodia
Foued Hamza & Slaheddine Selmi
To cite this article: Foued Hamza & Slaheddine Selmi (2016): Co-occurrence and commensal
feeding between Little Egrets Egretta garzetta and Eurasian Spoonbills Platalea leucorodia, Bird
Study, DOI: 10.1080/00063657.2016.1238035
To link to this article: http://dx.doi.org/10.1080/00063657.2016.1238035
Published online: 29 Sep 2016.
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Co-occurrence and commensal feeding between Little Egrets Egretta garzetta and
Eurasian Spoonbills Platalea leucorodia
Foued Hamza and Slaheddine Selmi
Département des Sciences de la Vie, Faculté des Sciences de Gabès, Université de Gabès, Gabès, Tunisia
ABSTRACT
Capsule: The spatial distribution and feeding efficiency of Little Egrets Egretta garzetta wintering in
the gulf of Gabès, Tunisia, are affected by a commensal association with the Eurasian Spoonbills
Platalea leucorodia.
Aims: To investigate the role of the interspecific interaction between Little Egrets and Eurasian
Spoonbills in shaping the spatial distribution and feeding efficiency of Little Egrets.
Methods: Using count and behavioural data, we examined the co-occurrence of these species in
flocks, and compared the foraging efficiency of Little Egrets feeding with Eurasian Spoonbills
with that of solitary Little Egrets.
Results: We found that the presence of Eurasian Spoonbills doubled the chance of Little Egrets
being present. Within mixed flocks, the number of Little Egrets increased with the number of
Spoonbills. Moreover, Little Egrets foraging in association with Eurasian Spoonbills took fewer
steps, had higher pecking rates and higher prey intake rates than solitary Little Egrets.
Conclusion: Little Egrets appear to obtain foraging efficiency benefits by following Eurasian
Spoonbills. This interaction seems to play a role in determining the spatial distribution of Little
Egrets.
ARTICLE HISTORY
Received 14 April 2016
Accepted 7 September 2016
Commensal foraging is a strategy commonly observed in
birds (e.g. Grubb 1976, Kushlan 1978, Davis 1985,
Källander 2005, King & Cowlishaw 2009,D’Angelo &
Sazima 2014). In this association, a ‘follower’species
feeds on the prey disturbed by a ‘beater’species,
without any foraging benefit or prejudice to the beater
(Dickman 1992, Schaefer & Fagan 2006, Herring &
Herring 2007). Typical benefits to the follower species
are an increase in foraging success, through increased
probabilities of prey detection and capture (Kushlan
1978, Bennett & Smithson 2001), and the decrease in
energy expenditure when searching for prey (Kushlan
1978, Russell 1978).
Previous studies have highlighted that commensal
foraging is frequent among wading birds occurring in
mixed-species flocks (Kushlan 1978, Davis 1985,
Bennett & Smithson 2001, Herring & Herring 2007, Fox
& Young 2012). However, the role of this interspecific
interaction in shaping the foraging ecology, habitat use
and spatial distribution of associated species remain
poorly studied. Here, this issue is investigated using data
on the Little Egret Egretta garzetta and Eurasian
Spoonbill Platalea leucorodia wintering in the gulf of
Gabès, in southeast Tunisia.
The Little Egret has been described as a follower
species in a number of circumstances (e.g. Reynolds
1965, Connor 1979, Kyle 2005). It is an opportunistic
predator that forages on a variety of aquatic prey,
including small fishes and invertebrates, and uses
visual cues for hunting (Voisin 1991, Fasola et al.
1993, Fasola 1994, Kushlan & Hancock 2005, Wood
& Stillman 2014). The typical feeding technique of
Little Egrets consists of walking through shallow
water with frequent halts to stand and wait for prey
to become visible (Hafner et al. 1982, Voisin 1991,
Tojo 1996, Phalan 1997,Nefla & Nouira 2016).
However, Little Egrets are often seen stirring the
sediment with their feet or running through the
water with raised wings to disturb prey (Voisin 1991,
Phalan 1997). They are also known to make use of
opportunities provided by other birds disturbing
fishes while foraging (Reynolds 1965, Fraser 1974,
Connor 1979, Kyle 2005). In contrast, different
spoonbill species have previously been described as
beater species in numerous feeding associations with
egrets (Reynolds 1965, Russell 1978, Connor 1979,
Kyle 2005). Indeed, spoonbills prey on small
invertebrates and fishes captured by sweeping the bill
© 2016 British Trust for Ornithology
CONTACT Foued Hamza fouedhamza2010@gmail.com Département des Sciences de la Vie, Faculté des Sciences de Gabès, Université de Gabès, Bloc de
recherche (Biologie, 1er étage), Zrig, 6027 Gabès, Tunisia
BIRD STUDY, 2016
http://dx.doi.org/10.1080/00063657.2016.1238035
into shallow water and mud, using tactile cues rather
than visual cues for prey detection and hunting
(Hancock et al. 1992, Matheu & del Hoyo 1992).
In this study, we used count and behavioural data on
Little Egrets and Eurasian Spoonbills to explore their
possible commensal association and to investigate the
possible roles of Eurasian Spoonbills in shaping the
distribution, abundance and feeding efficiency of Little
Egrets. More specifically, we addressed the following
questions: (1) Does the presence of Eurasian Spoonbills
increase the probability of Little Egrets being present in
that site? (2) Within occupied sites, are the numbers of
Little Egrets and Eurasian Spoonbills positively
correlated? (3) Do solitary Little Egrets expend greater
effort in prey searching and obtain lower prey intake
rates compared to Little Egrets associated with
Eurasian Spoonbills? (4) Does the feeding success of
Little Egrets associated with Eurasian Spoonbills vary
according to their relative number and their position in
the mixed flock?
Methods
Study area and species
Field work was conducted in the intertidal areas of the
Gulf of Gabès, in southeast Tunisia. The gulf has the
largest tides in the Mediterranean, with tidal
amplitude ranging between 0.8 and 2 m in neap and
spring tides, respectively (Pérez-Domingo et al. 2008).
The gulf is also recognized as an important wintering
area for Palearctic waterbirds, including the Eurasian
Spoonbill and Little Egret (van Dijk et al. 1986,
Smart et al. 2007, Hamdi et al. 2008). In this area,
the Eurasian Spoonbill is a regular wintering visitor,
while the Little Egret is known to breed in some
isolated islets but its abundance increases during
winter with the arrival of wintering birds (Isenmann
et al. 2005).
Like many wading birds wintering in the area, both
species are known to feed at low tide, using tidal
channels and pools as feeding sites (Hamza & Selmi
2015, Hamza et al. 2015). In these constantly
immersed tidal channels and pools, the sediment is
muddy and hosts an important invertebrate biomass,
including crustaceans, annelids and bivalves
(Pérez-Domingo et al. 2008), thus offering abundant
and accessible prey for the Eurasian Spoonbill (Hamza
& Selmi 2015, Hamza et al. 2015). Moreover, at low
tides, high numbers of juvenile fishes are stranded in
the tidal channels and pools, providing feeding
opportunities for piscivorous wading birds, such as the
Little Egret (Hamza & Selmi 2015, Hamza et al. 2015).
Data collection
Bird surveys
In order to investigate the co-occurrence of Little Egrets
with Eurasian Spoonbills at a relatively large spatial scale,
we surveyed the two species at 50 sites between Kneïs
islands (34°22′N, 10°15′E) to the north and Boughrara
lagoon (33°41′N, 10°40′E) to the south, along 125 km
of coastline in the central part of the gulf of Gabès,
Tunisia. Survey sites were distant from one another by
approximately 2.5 km. During the period between 10
December 2012 and 31 January 2013, each site was
visited five times at different dates for bird counting, so
that a total of 250 counts have been conducted. All
counts were conducted at low tide and usually by
the same observer (F. Hamza). During each count, the
observer used an elevated location close to the
coastline to record the number of Eurasian spoonbills
and Little Egrets, with the aid of a spotting scope or
binoculars. Date and time of day were also recorded.
Behavioural observations
We conducted behavioural observations on solitary Little
Egrets and those occurring in mixed flocks with Eurasian
Spoonbills. A mixed flock was defined as a close
association of at least one Little Egret with at least one
Eurasian Spoonbill (less than one meter apart) that
moved together in the same direction. These
behavioural observations have been conducted in
Gourine beach (33°39′N, 10°33′E), at the southern
part of the Gulf of Gabès. This site was selected to
carry out these observations because it was constantly
occupied by the two species of study, and also because
suitable observation posts were available at the
shoreline which facilitated the monitoring of focal
birds. All observations were carried out at low tide.
Once a mixed flock was detected, the number of
individuals of each species was first recorded. We
waited a few minutes before collecting data to allow
birds to become habituated to our presence, then one
actively foraging Little Egret was randomly selected
and its position within the flock noted. Two position
classes were distinguished: central (i.e. the focal bird
was inside the flock and surrounded by Eurasian
Spoonbills) versus peripheral (i.e. the focal bird was at
the outer edge of the flock). This focal individual was
observed for two minutes, using a telescope, and the
following behavioural variables were recorded: the
number of steps, the number of pecks and the number
of successful pecks (pecks with a food item seen to be
taken). The same parameters were immediately
2F. HAMZA AND S. SELMI
recorded on a solitary Little Egret feeding in the same
tidal channel or pool but situated some tens of meters
away from the mixed flock. This procedure provided
us with paired behavioural observations on feeding
Little Egrets (solitary versus associated with
spoonbills). All observations were recorded by the
same observer speaking into a recorder. We are aware
that because the monitored birds were not marked, a
possible problem of pseudoreplication might have
occurred in our data. However, in order to minimize
this potential bias we actively avoided repeated
sampling of the same individuals, by selecting
subsequent subjects situated in different flocks, so that
a single Little Egret was monitored per flock.
Statistical analysis
We first used the count data to investigate the
importance of Eurasian Spoonbills in shaping the
distribution and abundance of Little Egrets, while
accounting for the possible effects of habitat features,
date and time of day. Habitat features were assessed
using already published results of a Principal
Component Analysis that we conducted on a set of
environmental variables measured in the same sites
during the same period of study (see Hamza & Selmi
2015 for a full description). In summary, two factors
accounting together for 70% of the original variance
were retained. PC1 (47% of the original variance) was
positively correlated with intertidal flat width, number
of tidal channels, seagrass cover, mud content of the
sediment and organic matter of the sediment. PC2
(23% of the original variance) represents an axis of
increasing human disturbance, as it was positively
correlated with the number of humans and the rate
of site occupancy by humans (see Hamza & Selmi
2015).
We used a generalized linear mixed model (GLMM),
with a logit link function and binary distribution, to
assess the relevance of Eurasian Spoonbill presence in
predicting the occurrence probability of the Little
Egret. In this model, habitat features (PC1 and PC2),
date (number of days after the first survey visit) and
time of day (centred since sunrise) were also
considered as fixed effects, and site as a random effect.
A second GLMM, with an identity link function and
normal distribution, was also conducted to assess the
relationship between Little Egret number (log-
transformed) and Eurasian Spoonbill number (log-
transformed), while accounting for PC1, PC2, date and
time of day as fixed effects, and site as a random effect.
Moreover, in order to describe the structure of mixed
flocks we compared the numbers of followers (Little
Egrets) and beaters (Eurasian Spoonbills) by means of
a paired t-test.
Using behavioural data on the monitored Little Egret
pairs, we investigated whether the number of steps, the
number of pecks, the number of successful pecks, the
number of pecks per step (number of pecks/number of
steps), the number of successful pecks per step (number
of successful pecks/number of steps) and the pecking
success (number of successful pecks/number of pecks)
differed significantly between solitary Little Egrets and
those associated with Eurasian Spoonbills, using paired
t-tests. We also calculated, for each monitored pair, the
rate of difference between solitary Little Egret and that
associated with Spoonbills, regarding each of the above
cited foraging variables (X), as (X
a
−X
s
)/X
s
,withX
s
being the value recorded for the solitary Little Egret and
X
a
the value recorded for the one associated with
Eurasian Spoonbills. These values were then used to
investigate whether the extent of within-pair difference
varied according to the position of the Little Egret
associated with Eurasian Spoonbills in the mixed flock
(two classes: central versus peripheral) and the number
of Little Egrets per Eurasian Spoonbill, using analysis of
covariance (ANCOVA).
All models were conducted using the GLIMMIX
procedure in SAS (SAS Institute, 2008). In all models,
the ratio of the chi-square statistic and its degrees of
freedom was close to one (between 0.55 and 1.84),
indicating that the variability in our data has been
properly modelled and that there was no residual
overdispersion.
Results
Effects of Eurasian Spoonbills on the occurrence
and abundance of Little Egrets
During our 250 counts, the Eurasian Spoonbill was
recorded 118 times (47%) and the Little Egret 100
times (40%). The two species occurred together in
mixed flocks in 74 records (30%). Within these mixed
flocks, the number of Eurasian Spoonbills ranged from
1 to 94 (mean ± se = 26 ± 3), while the number of Little
Egrets varied between 1 and 66 (mean ± se = 11 ± 1).
The numbers of Eurasian Spoonbills minus the
number of Little Egrets occurring together in mixed
flocks ranged from −14 to 77 (mean ± se = 15 ± 3) and
showed significantly higher numbers of Eurasian
Spoonbills compared to Little Egrets (paired t-test:
t
47
= 6.55, P< 0.0001).
Using the entire count data, the results of GLMM
showed that Little Egret occurrence probability was
significantly greater on larger, more complex and
BIRD STUDY 3
productive sites (positive values of PC1; Table 1). They
also showed that Eurasian Spoonbill presence provided
a significant predictor of the occurrence probability of
the Little Egret (Table 1). According to this model, the
estimated occurrence probability of the Little Egret was
twice as large at sites where the Eurasian Spoonbill was
present (mean ± se = 0.552 ± 0.072) compared to sites
where the Eurasian Spoonbill was absent (mean ± se =
0.229 ± 0.053). Human disturbance (PC2), date and
time did not provide significant predictors of Little
Egret occurrence probability (Table 1).
Considering the subset of data on mixed flocks, we
found that the number of Little Egrets was negatively
affected by the intensity of human disturbance (PC2)
but positively related to the number of Eurasian
Spoonbills (Table 1). Habitat quality (PC1), date and
time of day had no significant effects on the number of
Little Egrets associated with Eurasian Spoonbills
(Table 1).
Effects of Eurasian Spoonbills on the foraging
behaviour and success of Little Egrets
We were able to conduct paired behavioural observations
on 62 Little Egrets associated with Eurasian Spoonbills in
mixed flocks and 62 solitary Little Egrets foraging in the
same area at the same time. All investigated feeding
variables differed significantly between solitary Little
Egrets and Little Egrets associated with Eurasian
Spoonbills (Table 2,Figure 1). Solitary Little Egrets
performed a higher rate of steps while foraging but had
lower pecking rates, and had significantly lower
pecking success than Little Egrets associated with
Eurasian Spoonbills (Table 2,Figure 1). However, the
extent of these differences did not vary significantly
according to the position of the Little Egret within the
mixed flock and the number of Little Egrets per
Eurasian Spoonbill (Table 3).
Discussion
The aim of our study was to investigate the role of the
interspecific interaction between Little Egrets and
Eurasian Spoonbills in shaping the spatial distribution,
abundance and feeding efficiency of Little Egrets
wintering in the Gulf of Gabès.
Our results first showed that Little Egrets occurred
more frequently in large mudflats crossed by large
numbers of tidal channels and pools that provided
suitable foraging sites at low tide. Accounting for these
effects of habitat structure, the presence of Eurasian
Spoonbills was found to double the probability of Little
Egrets being present. Furthermore, within occupied
sites, the number of Little Egrets, although lower in
areas where human presence was more frequent,
increased with the number of Eurasian Spoonbills.
Overall these results suggest that besides habitat
features, the presence and abundance of the Eurasian
Spoonbill plays an important role in shaping the
distribution and abundance of the Little Egret in the
Gulf of Gabès and seems to constitute a key factor in
the process of feeding site selection. Indeed, the
behaviour of following exhibited by Little Egrets and
their tendency to make use of feeding opportunities
offered by Eurasian Spoonbills seem to be an
important strategy to increase food intake and decrease
energy expenditure, thus improving foraging efficiency.
Table 1. Results of GLMMs of Little Egret occurrence probability
and number as functions of Eurasian Spoonbill presence (two
classes: presence = 1, absence = 0) and number, accounting for
habitat features (PC1 and PC2), date and time of day as fixed
effects and site as a random effect.
β±se tP
Little Egret occurrence probability
Intercept −1.513 ± 0.503 −3.01 0.0042
Eurasian Spoonbill presence 1.426 ± 0.429 3.31 0.0011
PC1 0.565 ± 0.236 2.39 0.0176
PC2 −0.147 ± 0.202 −0.73 0.4688
Date 0.001 ± 0.010 0.11 0.9134
Time of day 2.164 ± 2.099 1.03 0.3040
Little Egret number
Intercept 0.774 ± 0.471 1.64 0.1140
Eurasian Spoonbill number 0.336 ± 0.153 2.20 0.0333
PC1 0.242 ± 0.188 1.28 0.2056
PC2 −0.359 ± 0.147 −2.45 0.0182
Date −0.005 ± 0.006 −0.86 0.3936
Time of day −0.924 ± 1.712 −0.54 0.5920
Table 2. Statistics of measured foraging variables and results of comparisons between solitary Little Egrets (S) and those associated
with Eurasian Spoonbills (A). n= 62 paired observations of Little Egrets. Variables were recorded in observation periods of 2 minutes.
Solitary Egret (S)
Egret associated with
Spoonbills (A) Difference (A–S) Paired t-test
Range Mean ± se Range Mean ± se Range Mean ± se tP
Number of steps 71–124 96.94 ± 1.44 11–60 33.03 ± 1.09 −104–32 −63.90 ± 1.81 −35.31 <0.0001
Number of pecks 0–4 1.81 ± 0.14 0–9 3.60 ± 0.24 −3–6 1.79 ± 0.22 7.98 <0.0001
Number of successful pecks 0–2 0.84 ± 0.09 0–6 2.40 ± 0.18 −1–5 1.56 ± 0.18 8.86 <0.0001
Number of pecks per step 0–0.04 0.02 ± 0.00 0–0.33 0.11 ± 0.01 −0.02–0.32 0.10 ± 0.01 12.06 <0.0001
Number of successful pecks per step 0–0.02 0.01 ± 0.00 0–0.21 0.08 ± 0.01 −0.01–0.20 0.07 ± 0.01 11.30 <0.0001
Pecking success 0–1 0.47 ± 0.04 0–1 0.68 ± 0.03 −0.75–1.00 0.20 ± 0.06 3.40 0.0013
4F. HAMZA AND S. SELMI
This hypothesis was also supported by our behavioural
observations.
Little Egrets associated with Eurasian Spoonbills
performed more attempts to capture prey and were
more successful than solitary Little Egrets feeding in
the same habitat at the same time. The feeding
technique used by the Eurasian Spoonbill consists of
immersing its bill through shallow water and sweeping
it from side to side. This behaviour is likely to disturb
cryptic prey, making them more prone to predation,
thus increasing hunting attempts and pecking success
of Little Egrets. Moreover, within mixed flocks, Little
Egrets spread themselves around Eurasian Spoonbills
and walked slowly until a cryptic prey was disturbed
by a Eurasian Spoonbill. By contrast, solitary Little
Egrets generally walked rapidly through shallow water
in order to detect active prey, thus moving more and
deploying greater effort. Although we did not quantify
energetic costs, we can suppose that by walking less,
Little Egrets foraging in association with Eurasian
Spoonbills expend less energy than solitary Little
Egrets. This hypothesis is consistent with the
conclusions of several authors who proposed that
wading birds experience a reduction in energy
expenditure while feeding in association with other
wading birds (Dinsmore 1973, Grubb 1976, Kushlan
1978, Russell 1978). However, the opposite trend has
also been observed (Bennett & Smithson 2001).
Overall, our results are in accordance with the
findings of previous studies on the associations
between egrets and different wading bird species, such
as the White Ibis Eudocimus albus (Kushlan 1978),
Roseate Spoonbill Platalea ajaja (Russell 1978) and
African Spoonbill Platalea alba (Reynolds 1965,
Connor 1979, Kyle 2005), as well as with different
herbivorous mammal species (e.g. Dinsmore 1973,
Grubb 1976, Fernandez et al. 2014). In these mixed-
species associations, egrets increase their foraging
efficiency through exploitation of prey items disturbed
by the beater species. These findings stress that the
commensal association with other beater species
represents a common behavioural strategy in Ardeidae,
allowing them to maximize foraging efficiency. This
confirms the opportunistic nature and ecological
flexibility of Ardeidae species when it comes to
foraging (Voisin 1991, Kushlan & Hancock 2005).
Because of possible food competition among Little
Egrets occurring in the same flock, we hypothesized
that the benefits derived from commensal feeding may
depend on the relative numbers of Little Egrets and
Eurasian Spoonbills. Indeed, intraspecific aggression is
known to limit the advantages gained by followers in
commensal associations (Grubb 1976). Similar trends
have also been reported in other interspecific
associations between birds, such as kleptoparasitism
(Wood et al. 2015). We also expected the position of a
Little Egret within the mixed flock to affect its foraging
benefits through possible effects on the probability of
detecting prey disturbed by Eurasian Spoonbills.
However, our results gave no support to these
hypotheses as no feeding metrics varied significantly
with the position of the commensal Little Egret within
Figure 1. Mean (±se) differences in the rates of foraging
variables between Little Egrets associated with Eurasian
Spoonbills and solitary Little Egrets. Positive values show that
Little Egrets associated with Eurasian Spoonbills have higher
rates for the variable than solitary Little Egrets. Count
differences are for observation periods of 2 minutes.
Table 3. Results of ANCOVAs of the extent of differences between solitary Little Egrets and those associated with Spoonbills as functions
of Little Egret position within the mixed flock (two classes: central = 1, peripheral = 0) and the number of Little Egrets per Spoonbill.
Variables were recorded in observation periods of 2 minutes.
Intercept Position Egrets per Spoonbill
β±se tPβ±se tPβ±se tP
Number of steps −0.67 ± 0.02 −29.65 <0.0001 −0.00 ± 0.03 −0.14 0.8873 0.01 ± 0.01 0.87 0.3872
Number of pecks 0.61 ± 0.24 2.54 0.0140 0.30 ± 0.32 0.93 0.3563 0.14 ± 0.15 0.94 0.3536
Number of successful pecks 0.80 ± 0.38 2.14 0.0390 −0.23 ± 0.50 −0.46 0.6462 0.28 ± 0.21 1.34 0.1882
Number of pecks per step 4.50 ± 0.84 5.34 <0.0001 1.09 ± 1.14 0.96 0.3409 0.04 ± 0.51 0.08 0.9360
Number of successful pecks per step 5.43 ± 1.47 3.73 0.0006 −1.05 ± 1.96 −0.54 0.5936 0.52 ± 0.83 0.63 0.5323
Pecking success 0.17 ± 0.21 0.80 0.4314 −0.26 ± 0.28 −0.95 0.3496 0.07 ± 0.12 0.62 0.5399
BIRD STUDY 5
the mixed flock and the number of Little Egrets per
Eurasian Spoonbill.
Finally, it is noticeable that the benefits gained by
Little Egrets from the association with Eurasian
Spoonbills may also vary according to a number of
factors that have not been considered in our study. In
particular, we believe that further research should
investigate the possible effects of Eurasian Spoonbill
age on the foraging benefits gained by Little Egrets.
Indeed, because of their greater experience, adult
Eurasian Spoonbills could be assumed to select more
suitable feeding sites, thus providing more feeding
opportunities to Little Egrets, than young ones.
Moreover, the possible effects of competition with
other follower species should also be considered.
Indeed, it has previously been suggested that when
several follower species are associated together with a
beater species, the feeding benefits gained by the
individuals of the competitively inferior species are
reduced (Russell 1978). Investigations of these issues
are likely to provide important information to more
profoundly understand the interaction between Little
Egrets and Eurasian Spoonbills.
Acknowledgements
We wish to thank Fadhel Zaabi, Omar Khalbous, Habib
Msilini and the Fraj and Msilini families for their helpful
logistical support and accommodation during field work. We
also thank the Editor, Dr Ian Hartley, the Associate Editor
and two anonymous reviewers for their valuable comments
on an earlier version of the manuscript.
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BIRD STUDY 7
