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KLEPTOPARASITISM AND TEMPORAL SEGREGATION OF SYMPATRIC
CORVIDS FORAGING IN A REFUSE DUMP
R.
—El cleptoparasitismo, definido como la acción de robar comida a otros individuos de la misma o de diferentes especies,
es frecuente en las aves y representa una forma de competencia directa que podría influir sobre la estructura de las comunidades.
Evaluamos esta idea analizando el comportamiento de forrajeo y los patrones espacio-temporales de uso de un vertedero en cuatro
especies de córvidos (Corvus frugilegus, Corvus corone, Corvus monedula y Pica pica). Corvus corone mostró un peculiar grado de
especialización en el cleptoparasitismo, dedicando el mayor tiempo a vigilar desde la periferia del vertedero y atacando a otros individuos
en lugar de buscar directamente el alimento entre las basuras. En invierno, cuando la abundancia de córvidos fue más elevada, las especies
se segregaron mediante diferentes horarios de visita al vertedero, siendo C. frugilegus y C. monedula las más abundantes durante las
primeras horas del día, C. corone durante la mitad de la mañana y Pica pica durante las primeras horas de la tarde. Sugerimos que el
cleptoparasitismo jugó un papel en determinar la agregación temporal de las especies en el vertedero. Por una parte, C. corone coincidió
en el patrón diario de abundancia de sus principales hospedadores (Sturnus spp.), aumentando sus oportunidades de cleptoparasitarlos.
Por otra parte, la llegada tardía de Pica pica les previno de superponerse con C. corone, reduciendo el riesgo de ser robados y por lo
tanto aumentando la eficiencia de forrajeo. La segregación temporal de especies ha sido descrita raramente entre los vertebrados, pero
nuestros resultados sugieren que puede ser un mecanismo importante de coexistencia de especies cuando los recursos se encuentran
concentrados espacialmente.
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e Auk 126(3):566−578, 2009
e American Ornithologists’ Union, 2009.
Printed in USA.
e Auk, Vol. , Number , pages −. IS SN -, electron ic ISSN -. by e A merican Or nithologi sts’ Union. A ll rights r eserved. Ple ase direc t
all requests for permission to photocopy or reproduce article content th rough the University of Cali fornia Press’s Rights and Permi ssions website, http://www.ucpressjournals.
com/reprintInfo.asp. DOI : . /auk . .
Cleptoparasitismo y Segregación Temporal de Especies Simpátricas de Córvidos durante
el Forrajeo en un Vertedero
Vi t t o r i o Ba g l i o n e 1, 3 a n d da n i e l a Ca n e s t r a r i 2
1Department of Agroforestry, University of Valladolid, Avda. de Madrid 44, 340 04 Palencia, Spain; and
2Department of Animal Biology, Faculty of Science, University of Granada , University Campus Fuente Nueva, 18071 Granada, Spain
3E-mail: baglione@agro.uva.es
A.—Kleptoparasitism, in which an individual steals food from other individuals of the same or a different species, is frequent
in birds and represents a form of direct competition that can potentially influence the structure of communities. We addressed this idea
by analyzing the foraging behavior and the spatiotemporal patterns of use of a refuse dump by four species of corvids: the Rook (Corvus
frugilegus), Ca rri on Crow (C. corone), E ur asi an Jac kda w (C. monedula), an d Eu rop ea n M agp ie ( Pica pica). Carrion Crows showed a unique
degree of specialization in kleptoparasitism, allocating most of their time to scanning from the periphery of the dump and attacking
other individuals rather than searching directly for food on the refuse. During winter, when the presence of corvids was highest, the
species segregated through different timing of visits to the dump: Rooks and Eurasian Jackdaws were most abundant in the early hours,
Carrion Crows in the middle of the morning, and European Magpies in the early afternoon. We suggest that kleptoparasitism played a
role in shaping the temporal assemblage of species in the dump. On one hand, Carrion Crows matched the daily pattern of abundance
of their main hosts, the starlings (Sturnus spp.), thus increasing their opportunities for kleptoparasitism. On the other hand, European
Magpies’ delayed arrival prevented overlapping with Carrion Crows, which reduced their risk of being robbed and, therefore, enhanced
the efficiency of foraging. Temporal segregation of species has rarely been reported among vertebrates, but our results suggest that it may
be an important mechanism of coexistence on spatially clumped food resources. Receive d July , accepted Feb ruar y .
Key words:
corvids, Corvus spp., European Magpie, kleptoparasitism, Pica pica, segregation of species, temporal niche partitioning.
K
theft of food or other valuable re-
sources from hosts of the same or different species (Buckley ).
It occurs in a large variety of animals, including mollusks (Zamora
and Gómez , Iyengar ), insects (Filippi et al. ),
arachnids (Koh and Li ), fishes (Hamilton and Dill ), rep-
tiles (Cooper and Pérez-Mellado ), mammals (Gorman et al.
, Di Bitetti and Janson ), and birds (Brockmann and Bar-
nard ). In birds, kleptoparasitsm is nonrandomly distributed
among taxa (Morand-Ferron et al. ), being most frequent in
the order Pelicaniformes (where it has been described in .% of
species), in Falconiformes (.% of species), and in Char-
adriformes (.% of species). Kleptoparasitism is rare among
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Passeriformes other than corvids, in which it has been described
in .% of species (Morand-Ferron et al. ). Unlike the
five species of frigatebirds (Fregata spp.), which are specialized
kleptoparasites (Brockmann and Barnard ), most avian spe-
cies use robbing tactics facultatively, typically when there is a high
concentration of potential hosts on a predictable source of food
or when food is in short supply (Brockmann and Barnard ).
Under these circumstances, kleptoparasitism can become the
prevalent foraging technique and can seriously threaten hosts.
Well-known cases include larids (Larus spp.) stealing food from
puffins (Fratercula spp.) when the latter return to breeding col-
onies to feed their young, which substantially reduces the hosts’
reproductive success (St. Clair et al. , Finney et al. ), and
Spotted Hyenas (Crocuta crocuta) driving African Wild Dogs
(Lycaon pictus) to local extinction by stealing their kills (Gorman
et al. ).
ese examples show that kleptoparasitism can potentially
influence the structure of species communities, playing a role
similar to that of predation or other kinds of competition for re-
sources. However, studies on kleptoparasitism have focused
mainly on its costs and benefits in comparison with other feeding
techniques (Ha and Ha ), and little is known on how this be-
havior influences species coexistence and niche partitioning. As
a result, although kleptoparasitism is reasonably well understood
both theoretically and empirically in the context of optimal-for-
aging theory, its function in shaping communities is still largely
unknown.
Refuse dumps meet most conditions that favor the occur-
rence of kleptoparasitism in birds, namely predictable availabil-
ity of food, large and visible food items, and high concentration of
potential hosts (Brockmann and Barnard ). Indeed, some in-
stances of food stealing have been reported in this kind of anthro-
pogenic environment (Steele and Hockey , Galván ). A
refuse dump in northern Spain, near the city of León, is regularly
used by birds, in particular by four species of corvids: the Carrion
Crow (Corvus corone), Rook (C. frugilegus), Eurasian Jackdaw (C.
monedula), and European Magpie (Pica pica). ese species have
similar ecology in terms of diet, habitat selection, and feeding be-
havior (Waite b), and several studies have addressed some
mechanisms of niche partitioning that allow them to coexist in
natural environments (Waite a, b; Rolando ).
Our aim was to investigate the occurrence of kleptoparasit-
ism in the corvid guild and to determine whether robbing behavior
plays a role in shaping the patterns of spatial and temporal use of
the dump at the interspecific level. We compared the feeding strat-
egies of the four species, their use of different parts of the dump,
their daily and annual cycle of abundance, the frequency and suc-
cess rate of their kleptoparasitism, and their choice of hosts.
Me t h o d s
Refuse dump, avian community, and bird counting.—e dump
tha t we stu di ed ( °′N, °′W) wa s op ene d in th e la te s a nd
served the city of León in northwest Spain. e dump was perma-
nently exposed, and the birds had access to the whole refuse area
(~. ha). Every day, new refuse was dumped on top of previous
layers and flattened mechanically. An area of ~. ha adjacent to
the dump (hereafter “periphery”) that was used for storing empty
containers and maneuvering trucks also was used by birds, mostly
for escaping machines working on the refuse or for resting. Other
than the four species of corvids, Spotless Starlings (Sturnus uni-
color) and European Starlings (S. vulgaris) were the most abun-
dant avian species.
From January until December , we visited the
dump approximately every other week (n = visits) to census
corvids with binoculars and a spotting scope from a single van-
tage point. Beginning in September , we counted starlings as
well. Counts started h after sunrise and were repeated every h
until dusk. e location of birds (refuse surface vs. periphery) was
recorded. e use of a voice recorder allowed a quick and uninter-
rupted scan of the dump, which was divided in six sectors. Dur-
ing the counts, which lasted ~ min, we recorded birds moving
across sectors and to and from the dump, to avoid double count-
ing. When we failed to keep track of moving birds, we aborted the
count and immediately began again (sometimes up to three or
four times). When starlings were present in the thousands, we had
to estimate their numbers separately, after counting corvids. e
two species of starlings are too similar to be differentiated during
a quick count, so we pooled their numbers. Correlations between
the daily maximum numbers of individuals of the different species
counted in the dump throughout the year were tested with Spear-
man rank correlation, and within-species differences in the num-
ber of individuals counted at different times of day were analyzed
with Kruskal-Wallis analysis of variance (ANOVA).
Foraging behavior.—Between November and February, we
conducted two kinds of behavioral observations of corvids for-
aging in the dump: focal sampling and ad-libitum recording of
kleptoparasitic interactions. Observations took place both in the
morning and in the afternoon, typically between bird counts,
avoiding the late hours when birds mainly engaged in pre-roost
social activities rather than foraging.
We used focal sampling to describe the foraging behavior
of the four corvid species. Focal individuals were followed for
≤ min, and their behavior was videotaped. Observations that
lasted ≤ min, because of the bird’s departure or for any other
reason, were discarded. We calculated the proportions of time
spent in five categories of behavior: moving, handling refuse
(picking items on a spot), scanning (vigilant posture with head
raised), flying, and resting (perching without scanning). Because
the food handled was rarely recognizable, food intake was as-
sessed as the frequency of swallows. To avoid biasing the sam-
ple toward individuals that displayed a particular behavior, we
chose individuals of each species according to the activity they
displayed when we first looked at them, following a sequence
that made the five behavioral categories equally represented. At-
tempted kleptoparasitism was recorded as well, taking note of
the species of the host, the direction of the attempt (focal indi-
vidual stealing food or being stolen from), and its outcome. We
defined an “attempt” at kleptoparasitism as a quick approach of
an individual to its target, either by flying, jumping, or walking,
overtly aimed at stealing the food that the latter was consum-
ing. is often involved pecking or other kinds of physical con-
tact. e attempt was considered successful if the initiator stole
the food or displaced the host from the feeding spot and took
over in handling the food. We sampled individuals of the
four species feeding on the refuse area and on the periphery
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(see details below). Although birds in the dump were unbanded,
th e hig h nu mbe rs m ade it u nlik ely th at i ndiv idu als wer e sa mpl ed
more than once. We therefore considered the focal samples sta-
tistically independent.
Besides focal sampling, we also scanned the refuse surface
and the periphery with binoculars to record attempted kleptopar-
asitism. For every instance observed (n = ), the identity of the
host was recorded, as well as the outcome of the attempt when
possible. To avoid biasing the sample, we distributed our scans
homogeneously over the whole dump. Because all corvids were
equally visible on the dump, these ad-libitum observations were
a suitable complement to the focal sampling.
To analyze feeding behavior, we used Kruskal-Wallis ANOVA
and Mann-Whitney U tests for comparisons involving only two
samples. We used chi-square tests for among-species differences
in host choice and kleptoparasitic success rate. To avoid predicted
frequencies <, it was sometimes necessary to delete data on Euro-
pean Magpies, as described below. Fisher’s exact test was used for
× tables of contingency.
Re s u l t s
Annual Cycle
e annual cycles of abundance in the dump varied among species
(Fig. A, B). Rooks and Eurasian Jackdaws showed annual max-
ima during the postbreeding periods (July–September). Carrion
Crows’ abundance peaked in winter and European Magpies were
most common in late summer and winter. All species showed a
sharp decrease during the breeding months (April–June). Most
birds at the dump in late autumn and winter (November–February)
were European and Spotted starlings, which together reached
peaks of ~, individuals simultaneously foraging on rubbish
(Fig. A). roughout the year, the numbers of Carrion Crows and
starlings were highly correlated (Spearman rank correlation, r =
., P < .; Fig. A), as were the numbers of Rooks and Eurasian
Jackdaws (r = ., P = .; Fig. B). Both correlations remained
significant when applying Bonferroni sequential correction for
multiple testing (Holm ).
Fig . 1. Maximum numbers of (A) starlings and Carrion Crows and (B) Eurasian Jackdaws, Rooks, and European Magpies recorded in the refuse dump
from 15 September 1992 until 1 December 1993. Every datum represents a day of censusing at the dump.
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Daily Cycle
e daily cycle of visits to the dump varied among corvid species
(Fig. B–E). In the cold months (November–February), Rooks
arrived en masse in the early morning, and most left within the
next h (Kruskal-Wallis ANOVA, difference among -h peri-
ods: H = ., df = , P < .). Eurasian Jackdaws also peaked
in the early morning (H = ., df = , P < .), but their pres-
ence was more constant throughout the day. Among the four spe-
cies, only European Magpies used the dump more intensively in
the afternoon (H = ., df = , P < .). Carrion Crows arrived
at the dump later in the morning than the other corvids (Fig. B),
typically when starlings also began to be abundant (Fig. A), and
their presence decreased sharply after midday (H = ., df = ,
P < .). During the rest of the year (March–October), Rooks and
Eurasian Jackdaws showed a peak of abundance at dusk (Kruskal-
Wallis nonparametric ANOVA, difference among -h periods
for the two species, respectively: H = ., df = , P < . and
H = ., df = , P < .; Fig. ), when they used the dump for
pre-roost gathering, with little foraging activity. Conversely, Eu-
ropean Magpie abundance did not show any significant variation
throughout the day (H = ., df = , P = .). e few Carrion
Crows that visited the dump during this period showed a peak in
the late morning (H = ., df = , P < .), as in winter.
Habitat Use and Winter Feeding Behavior
Rooks, Eurasian Jackdaws, and European Magpies were more
commonly seen in the refuse area, whereas Carrion Crows used
the per iph er y mo re i nt ens ivel y, a s sh own by t he ave rag e (± S E) p ro-
portion of individuals in this part of the dump at any bird count:
Carrion Crows, . ± .; Rooks, . ± .; Eurasian Jackdaws,
. ± . ; Eu ro pe a n M ag pi es , . ± . (Kruskal-Wallis ANOVA,
H = ., df = , P = ., n = ).
Feeding behavior on the refuse area.—e proportion of time
spent handling rubbish, moving, scanning, and flying significantly
differed among the four species (Kruskal-Wallis nonparametric
ANOVA, handling: H = ., P = .; moving: H = ., P < .;
scanning: H = . , P < .; flying: H = . , P = .; df = for all
analyses; Carrion Crow, n = ; Rook, n = ; Eu rasian Ja ckdaw, n =
; European Magpie, n = ; Fig. A). Carrion Crows spent most of
their time scanning and spent less time handling rubbish than the
other species. Rooks showed the highest overall frequency of swal-
low s (H = ., d f = , P < .; Fig. B) and the highest rate of food
intake when handling a rubbish item (average [± SE] frequency of
swallows per minute of handling rubbish: Rook, . ± .; Car-
rion Crow, . ± .; Eurasian Jackdaw, . ± .; European
Magpie, . ± .; Kruskal-Wallis ANOVA, H = . , P < .,
n = ). Carrion Crows showed the highest frequency of attempted
kleptoparasitism (H = ., df = , P < .; Fig. B), whereas Eur-
asian Jackdaws were more likely to be kleptoparasitized (H =
., df = , P < .; Fig. B). Neither Rooks nor Eurasian Jack-
daws showed differences in their foraging behavior on the dump
between morning and afternoon (none of the six variables mea-
sured was significant in a Mann-Whitney U-test; Carrion Crows
could not be tested because of the limited number of birds sam-
pled in the afternoon). Conversely, European Magpies proved to be
far more efficient during their afternoon peak (Fig. A, B), allocat-
ing more time to handling food (Mann-Whitney U-test, U = ,
Fig . 2. Average (± SE) number of (A) starlings, (B) Carrion Crows,
(C) Rooks, (D) Eurasian Jackdaws, and (E) European Magpies at the refuse
dump throughout a day. The timing of each count is indicated on the x
axis as number of hours after sunrise. For every corvid species, the dif-
ferences within each period of the year (autumn–winter and spring–sum-
mer) were significant (P < 0.05), with the exception of European Magpies
in spring–summer.
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P = .) and less to moving (U = , P = . ) a n d s c a n n i n g ( m a r g i n -
ally nonsignificant; U = , P = .), a nd ob tai ning a s ignifica ntly
higher intake of food (frequency of swallows, U = ., P = .).
Also, the European Magpies were less likely to be kleptoparasitized
in the afternoon than in the morning hours (U = ., P = .).
Feeding behavior on the periphery.—European Magpies were
rarely seen on the periphery of the dump and were, therefore, ex-
cluded from the analyses. Rooks and Eurasian Jackdaws used the
periphery mostly for resting (Kruskal-Wallis ANOVA, differ-
ence among species in the proportion of resting: H = ., df = ,
P < .; Carrion Crow, n = ; Rook, n = ; Eurasian Jackdaw,
n = ; Fig. A), although sometimes they used this area for han-
dling food items brought from the refuse area when disturbed by
machines at work on the dump. Unlike the other species, Carrion
Crows scanned most of the time (among species, H = ., df = ,
P = .; Fig. A) and showed the highest frequency of attempted
kleptoparasitism (H = . , df = , P < .; Fig . B ). ere wer e no
differences among species in the number of swallows obtained (H =
., df = , P = .; Fig. B).
Number of Aggressions and Host Choice
During both focal sampling and random sampling of birds forag-
i ng o n t he d um p, w e o bse r ved ag gr es sio ns in wh ich an in di vi d-
ual attempted to steal food handled by another bird of the same or
a different species. Of those, were initiated by Carrion Crows,
by Rooks, by Eurasian Jackdaws, and by European Mag-
pies. e two kinds of sampling returned very similar frequency
of attacks (see frequency of attacks per species in Fig. B and num-
ber of total attacks per species in Fig. for a qualitative compari-
son) and host choice (comparison of frequencies of attack per host
species between the two sampling methods: Carrion Crow, χ =
., df = , P = .; Rook, χ = ., df = , P = .; Eurasian Jack-
daw, χ = ., df = , P = .; European Magpie, χ = ., df = ,
P = .) and were therefore pooled. Carrion Crows and European
Magpies preferentially attacked starlings, whereas Rooks and Eur-
asian Jackdaws were more aggressive toward conspecifics (Fig. ).
Such differences among species in host choice were highly signifi-
ca nt (χ = ., df = , P < .; European Magpies were excluded
from the calculation to avoid expected frequencies <).
Unlike the other corvid species, Carrion Crows attacked more
often on the periphery of the dump (χ = . , df = , P < .) . e y
Fig . 3. Feeding behavior of focal individuals (sample sizes in parenthe-
ses) of the four corvid species in the refuse area. (A) Proportion of time
spent handling rubbish, moving, scanning, and flying. (B) Frequency of
swallows and of attacks made against and received from other birds for-
aging on the dump. Asterisks indicate significant differences between
species (P < 0.05).
Fig . 4. Foraging behavior of European Magpies (number of individuals
in parentheses) on the refuse area in the morning and in the afternoon.
(A ) Pr opor tion of t ime spe nt h and ling rubb ish, m oving , sc ann ing , an d fly -
ing. (B) Frequency of swallows and of attacks made against and received
from other birds foraging on the dump. Asterisks indicate significant
differences between morning and afternoon (P < 0.05).
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typically perched on a metallic fence (~ m high) on the periphery
and, from that vantage point, spotted potential victims handling
food brought from the refuse area. e attacks consisted of a fast
flight that usually ended on the ground but that also was sometimes
followed by an aerial pursuit. On the refuse area, Rooks and Eurasian
Jackdaws usually attacked birds foraging nearby on the ground, but
Carrion Crows often performed aerial attacks to reach more dis-
ta nt vic tims. Notably, C arrion Crows typica lly attacke d after a pro -
longed period of scanning from vantage points, whereas Rooks and
Eu ras ian Jac kdaw s see med to b e mor e opp ort uni sti c, t aki ng advan -
tage of occasional encounters, within the flock, with neighbors that
were handling food. In addition, Carrion Crows showed intimidat-
ing postures and physically aggressive contacts with the hosts more
often than the other species, whereas Eurasian Jackdaws often were
more st ealt hy when confro nted w ith l arger hosts.
No difference was found among species in the overall propor-
tion of successful attacks (χ = ., df = , P = .; result obtained
pooling data of all hosts species). e high number of aggressive ac-
tions by Carrion Crows allowed some further analysis for this spe-
cies. e proportion of successful attacks did not vary according to
Fig . 5. Feeding behavior of focal Carrion Crows, Rooks, and Eurasian
Jackdaws (sample sizes in parentheses) on the periphery of the dump.
European Magpies were rarely seen in this part of the dump and, there-
fore, were excluded from the analyses. (A) Proportion of time spent han-
dling rubbish, moving, scanning, flying, and resting. (B) Frequency of
swallows and of attacks made against and received from other birds for-
aging on the dump. Asterisks indicate significant differences between
species (P < 0.05).
Fig . 6. Host choice of four corvid species kleptoparasitizing in the dump
(number of attacks recorded in parentheses).
ho st sp eci es (χ = ., df = , P = . ; Eu ro pe an Mag pi e w as exc lu ded
from the analysis because of low sample size) and was not signifi-
cantly affected by the location in the dump (refuse area vs. periphery;
Fisher’s exact test, P = .; obt aine d by pooli ng dat a for all host spe -
cies). No difference between refuse area and periphery was found,
even when we restricted the analysis to Carrion Crows’ preferred
hosts, starlings (Fisher’s exact test, P = .) and Ro oks (P = . ).
di s c u s s i o n
Urban refuse is an abundant, high-energy, predictable food re-
source that is commonly used by wild populations of animals,
especially birds (Donázar , Pons and Migot , Olea and
Baglione ). When resources are clumped, individuals have
few options for reducing overlap in spatial distribution or food
choice, which are the niche dimensions along which species com-
monly segregate. Direct competition, of which kleptoparasitism is
an example, is likely to arise (Goldberg et al. ). In León’s dump,
all corvids kleptoparasitized other individuals, but there were im-
portant differences among species. We also observed that, even
in such conditions of food concentration, corvid species could re-
duce their overlap in dump use by temporal segregation, on both a
daily and a seasonal scale. Below, we first address patterns of klep-
toparasitism in the corvid guild, discussing the unique degree of
specialization exhibited by Carrion Crows. We then analyze the
role of kleptoparasitism in shaping the temporal segregation of
corvids at the dump.
Kleptoparasitism at the Dump
Among the four corvid species that used the refuse dump, Car-
rion Crows had the most peculiar feeding behavior, spatial distri-
bution in the dump (refuse area vs. periphery), and daily cycle of
abundance, which together indicate a degree of specialization in
kleptoparasitism. During winter, when their numbers were high-
est, Carrion Crows preferentially used the periphery of the dump
rather than foraging directly on the refuse. On the periphery, Car-
rion Crows mainly scanned and showed the highest frequency
of attempts at kleptoparasitism, in contrast to the other spe-
cies, which used this area mainly for resting. Carrion Crows also
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frequently attacked other birds on the refuse area and allocated
most of their time there to scanning rather than directly search-
ing for food. With regard to temporal distribution on the dump,
Carrion Crows’ daily cycle of abundance matched, to a remarkable
degree, that of their main hosts, the starlings, whose late arrival in
the morning was likely attributable to the large distance between
the dump and the riparian plantations of poplar (Populus spp.) in
southern León province where they roosted. We suggest that Car-
rion Crows synchronized their timing of visits to the dump with
that of the starlings. Alternative explanations seem unlikely. Be-
cause refuse is abundant and predictable (Pons and Migot )
and, hence, represents an ideal solution to the high energetic de-
mand after a cold night, we would have expected the abundance
of Carrion Crows to peak at dawn, like that of Rooks and Eurasian
Jackdaws, rather than later in the morning. e distance from
roost to dump could not account for the morning delay of Carrion
Crows, because they typically roosted communally with Rooks
and Eurasian Jackdaws near the dump (V. Baglione unpubl. data,
P. Olea and F. J. Purroy pers. comm.). Avoidance of competition
with other species also seems unlikely, because Carrion Crows are
dominant within this corvid guild (Bossema et al. ).
e correlation between the annual cycles of Carrion Crows
and starlings, characterized by highest abundance in winter,
could also reflect active kleptoparasite–host synchronization, but
alternative explanations are plausible. In particular, the absence of
Carrion Crows in the dump during the postbreeding period, when
other corvids are usually abundant, may be attributable to the fact
that they live in cohesive kin groups in this part of Spain (Bagli-
one et al. b) and leave the breeding territories only in winter
(Baglione et al. ), when food is in short supply.
Overall, our data indicate that, although kleptoparasitism
is part of the behavioral repertoire of all corvids, Carrion Crows
have reached the highest degree of specialization. Below, we ad-
dress some possible explanations for this pattern.
Why Carrion Crows?
It has been suggested that nutrition is not the sole factor driving
kleptoparasitism and that food theft can be involved in establish-
ing intraspecific social dominance (LeBaron and Heppner ).
In the present study, this hypothesis may apply to Rooks and Eur-
asian Jackdaws, which attacked mostly conspecifics, but it is un-
likely to explain the behavior of Carrion Crows, which usually
parasitized other species at the expense of direct search for food.
Interspecific dominance is also unlikely, because it cannot account
for Carrion Crows’ preference for starlings, which are not direct
competitors, nor for their synchronization with the daily cycle of
the starlings. erefore, we believe that kleptoparasitism in Car-
rion Crows must be interpreted as a true foraging technique.
e observed prevalence of kleptoparasitism in Carrion
Crows is surprising, considering that Carrion Crows, Rooks, Eur-
asian Jackdaws, and European Magpies share many ecological and
morphological features, in that all are generalist omnivorous birds
with strong beaks that have a tearing-edge typical of scavengers
and that all have rather similar foraging repertoires (Waite a).
e similarity is especially striking between Carrion Crows and
Rooks, which also are the same size and shape and have similar
flying abilities—and might be expected, therefore, to be equally
likely to be kleptoparasitic. Indeed, we found that Carrion Crows
and Rooks had the same success when stealing food; however,
Rooks seemed to be better foragers in the refuse area. Assuming
that the two species ingested food items of similar size and qual-
ity, Rooks’ higher frequency of swallows (Fig. B) and higher num-
ber of swallows obtained per piece of rubbish handled indicate a
more efficient use of refuse. Such efficiency, which could be re-
lated to natural digging habits of Rooks that may be helpful when
searching among refuse, may explain why Rooks are not special-
ized kleptoparasites.
An alternative explanation is that Carrion Crows possess
a larger behavioral flexibility than Rooks, which allows them to
increase the benefits of theft. Carrion Crows can adjust their so-
cial organization from social monogamy to kin-group living and
cooperative breeding (Baglione et al. b) in response to the
environment (Baglione et al. a, ). e Carrion Crows ad-
justed their daily cycle of use of the dump to that of starlings and
used the fence on the periphery of the dump in a unique way, start-
ing their attacks from above and probably improving the energetic
balance of theft. It is intriguing that in , in the same dump,
only % of the total number of Carrion Crows counted in
censuses were observed on the periphery (A. Reija pers. comm.),
whereas .% were thus observed in the present study. Although
a statistical comparison with our data is not possible because of
differences in methodology, this datum suggests, at least qualita-
tively, a modification of Carrion Crows’ foraging tactics over time
and a progressive specialization in kleptoparasitism. If Rooks lack
the behavioral plasticity of Carrion Crows, they may have been
incapable of increasing the profitability of food theft as compared
with direct search on the refuse area.
Temporal Segregation of Species: The Role of Kleptoparasitism
How species coexist in sympatry has been the focus of inten-
sive research for decades (for a pioneering, influential paper, see
Hutchinson ), and habitat and diet appeared from the begin-
ning to be the most important niche dimensions along which spe-
cies segregate (Lack , Schoener ). A sampling of recent
literature (–; see Appendix) confirmed this view. Of
studies on both vertebrate and invertebrate communities, re-
port on spatial segregation of species, and account for differ-
ences in diet or foraging behavior as mechanisms of coexistence.
Conversely, reports on temporal distributions of species, both
daily and seasonal, are uncommon ( studies of ) and seem even
rarer among terrestrial vertebrates ( studies of ). Nevertheless,
our data showed differences in the assemblage of corvids in the re-
fuse dump throughout the year and, remarkably, throughout the
day in winter, when all four species were abundant. In particular,
the daily activity patterns of Carrion Crows, which peaked late in
the morning, and European Magpies, which peaked in the early
afternoon, reduced the temporal overlapping of species on the
dump.
Previous studies have shown that kleptoparasitism can play
a role in shaping important behavioral patterns in birds—for
example, territorial behavior in Northern Harriers (Circus cya-
neus; Temeles ). An interesting question here is the extent
to which Carrion Crows’ kleptoparasitism, a form of direct com-
petition for resources, drove the observed winter daily patterns
of the corvid guild. Although both Rooks and Eurasian Jackdaws
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573
left the dump in the morning when Carrion Crows arrived, the
most parsimonious explanation of their daily cycle is that they
had satisfied the morning energetic demand and left to seek al-
ternative sources of food. Neither Rooks nor Eurasian Jackdaws
returned en masse to forage in the dump when Carrion Crows
had left. Furthermore, both species attended the dump in high
numbers and, therefore, diluted the risk of being robbed. Con-
versely, we suggest that European Magpies actively avoided klep-
toparasitism, especially by Carrion Crows, by shifting their peak
of activity toward the early afternoon. It may be argued that Eu-
ropean Magpies are the least likely to be attacked by Carrion
Crows (Fig. ) and that this weakens the avoidance hypothesis.
However, as in many species in which low rates of predation do
not necessarily imply that the actual risk of predation is low (Du-
rant ), the low frequency of Carrion Crows’ kleptoparasitic
attacks on European Magpies may indicate that the European
Magpies’ mechanism of avoidance is highly efficient, and not
that the level of competition is low. In this regard, it is interest-
ing to note the following. () In the afternoon peak, European
Magpies increased their foraging efficiency, engaging more in
handling potential food items and obtaining significantly more
food than in the morning. () Fewer European Magpies (≤)
were at the dump than other potential hosts of kleptoparasitism
and, therefore, they were less likely to dilute their risk of being
robbed; moreover, they are highly visible birds, they are subor-
dinate to Carrion Crows (Bossema et al. ), and they handled
rather large and visible food items while foraging at the dump,
which made them ideal hosts for kleptoparasites (Brockmann
and Barnard ). () As for Carrion Crows, the delay in arriv-
ing at the dump cannot be attributable to large roost-dump dis-
tan ces, beca use E uro pe an M ag pie usua ll y ro os ted nea r t he d um p
in winter (V. Baglione unpubl. data, P. Olea pers. comm.). And
most notably (), during spring and summer, when few Carrion
Crows were at the dump, the afternoon peak of abundance of Eu-
ropean Magpies disappeared and individuals attended the dump
more constantly throughout the day.
Our data suggest that kleptoparasitism has a role in shaping
the temporal distribution of corvids at the dump in winter, deter-
mining, on one hand, the delayed arrival of Carrion Crows in the
morning, to synchronize with their main hosts, and, on the other,
the peculiar afternoon peak of European Magpies that allowed
them to avoid aggression by kleptoparasites. Alternatively, Euro-
pean Magpies may have delayed their arrival to avoid competition
for hosts, given that they shared with Carrion Crows a preference
for starlings (Fig. ). However, the fact that European Magpies
decreased (though not significantly) the frequency of their klep-
to pa rasi tic atta ck s in the a ft erno on ( Fig . B ) se ems t o we ake n sup -
port for this hypothesis.
Although flexible adjustments of daily activity are common
among vertebrates (Beltrán and Delibes , Zalewski ) and
offer a potential immediate response to situations of direct com-
petition for resources, temporal segregation of species seems rare
among terrestrial vertebrates. e present study, however, sug-
gests that the temporal dimension of the niche can be important
in reducing species overlap and, to some extent, in preventing di-
rect competition. is mechanism may be more common than
previously thought, especially when species congregate on spa-
tially clumped food resources.
Ac k n o w l e d g M e n t s
We are grateful to D. C. Dearborn, J. J. Luque, J. Morand-Ferron,
and an anonymous reviewer for useful comments on the manu-
script and to Ayuntamiento of León for permission to work in the
refuse dump. e work was supported by the Spanish Ministry of
Education and Science (ref. CGL-/BOS), the “Ramón
y Cajal Program” (FEDER-FSE), and the Diputación de León (to
V.B.).
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ap p e n d i x . Review of 208 papers published between 1992 and 2007, returned by searching for “niche partitioning” or “species segregation” within the
kingdom Animalia in the Web of Knowledge (Thompson Reuters). Of those papers, 56 provided relevant information on the dimension of the niche
along which partitioning occurred. This appendix is not meant to be a comprehensive review of all works published on this topic, but rather a sample
to assess the relative importance of the different mechanisms of coexistence of species.
Orders and
families Species
Type of niche
partitioning
(intraspecific vs.
interpsecific)
Dimension of niche partitioning
ReferenceSpatial Temporal Diet
Feeding
behavior
Nematodes
Rhabditida Scottnema lindsayae and
Plectus antarcticus
Interspecific ×Nkem et al. 2006
Arachnids
Araneae Six species of Araneidae
and Tetragnathidae
Interspecific ×Ward and Lubin 1992
Insects
Plecoptera Nine species Interspecific × × Smith et al. 2000
Orthoptera:
Acrididae
Five dominant species Interspecific ×Lockwood et al. 1996
Coleoptera:
Cicindelidae
Cicindela circumpicta
and C. togata
Interspecific ×Hoback et al. 2000
Coleoptera:
Scarabaeldae
24 specie s Interspecific ×Verdú et al. 2006
Coleoptera:
Scolytinae
38 species Interspecific ×Jordal 2006
Hymenoptera:
Apidae
24 specie s Interspecific ×Biesmeijer and Slaa 2006
Hymenoptera Nectar-feeding ant communities
(43 species)
Interspecific ×Blüthgen and Fiedler 2004
Hymenoptera Seven species Interspecific × × Albrecht and Gotelli 2001
Lepidoptera:
Satyrinae
Heteropsis ssp. Interspecific ×Monte-Alegre et al. 2005
Lepidoptera:
Pieridae
Leptidea sinapis and L. reali Interspecific ×Amiet 2004
Diptera:
Cecidomyiidae
Izeniola obesula and
Stefaniola defoliata
Interspecific ×Dorchin 2006
Diptera:
Tephritidae
Ceratitis catoirii, C. rosa,
C. Capitata, and
Bactrocera zonata
Interspecific ×Duyck et al. 2006
Diptera Seventeen families from
freshwater wetlands
Interspecific × × × × Keiper et al. 2002
Crustaceans
Copepoda Large assemblage
of Scolecitrichidae
Interspecific ×Kuriyama and Nishida 2006
Copepoda Acartia clausi, Oithona
nana, Temora longicornis
and Euterpina acutifrons
Interspecific ×Guisande et al. 2002
Amphipoda Jassa falcata and J. marmorata Interspecific ×Karez and Ludynia 2003
(Continued )
Z, A.
. Seasonal and sexual variation in diel activ-
ity rhythms of Pine Marten Martes martes in the Białowieża
Nat ional Pa rk (Poland). Acta eriologica :–.
Z, R., J. M. G
. . Carnivorous plant–slug inter-
action: A trip from herbivory to kleptoparasitism. Journal of Ani-
ma l Ecol ogy :– .
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Ju l y 2009
—
Kl e p t o p a r a s i t i s m in sy m p a t r i C Co r V i d s
—
577
Orders and
families Species
Type of niche
partitioning
(intraspecific vs.
interpsecific)
Dimension of niche partitioning
ReferenceSpatial Temporal Diet
Feeding
behavior
Fish
Perciformes Pomacentridae and Labridae Interspecific ×Floeter et al. 2007
Perciformes Siganus rivulatus and S. luridus Interspecific ×Lundberg et al. 2004
Perciformes Eight species of chiclids Interspecific × × Genner and Turner 2005
Salmoniformes Salvelinus namaycush Intraspecific × × Morbey et al. 2006
Salmoniformes Salvelinus malma and
S. leucomaenis
Interspecific ×Nakano et al. 1999
Large assemblage of species Interspecific × × Herder and Freyhof 2006
Reptiles
Squamata Bothrops jararaca Intraspecific ×Furtado et al. 2006
Squamata Laticauda colubrina Intraspecific ×Shine et al. 2002
Squamata Morelia spilota imbricata Intraspecific ×Pearson et al. 2002
Amphibians
Caudata Ambystoma ssp. Interspecific ×Brodman and Jaskula 2002
Caudata Triturus alpestris Intraspecific × × Denoël and Joly 2001
Anura Rana esculenta complex Mother species
vs hybrids
×Pagano et al. 2001
Birds
Procellariiformes Thalassarche chrysostoma
and T. melanophrys
Interspecific ×Arata et al. 2003
Anseriformes Clangula hyemalis, Melanitta
nigra, and Aythya marila
Interspecific × × Kondratyev 1992
Anseriformes
and Gruiforme s
Anas strepera and Fulica
americana
Interspecific ×McKnight and Hepp 1998
Ciconiformes:
Ardeidae
Four species Interspecific ×Abbasi and Yahya
unpublished data
Falconiformes Circus cyaneus and C. pygargus Interspecific × × Garcia and Arroyo 2005
Falconiformes Accipiter novaehollandiae and
A. fasciatus
Interspecific ×Burton and Olsen 2000
Charadriiformes
and Gaviformes
Uria aalge and Cerorhinca
monocerata
Interspecific ×Lance and Thompson 2005
Coraciiformes Phoeniculus purpureus Intraspecific ×Radford and Du Plessis
2003
Piciformes Dendrocopos major
and D. medius
Interspecific ×Kosi´nski and Winiecki 2004
Piciformes Dendrocopos medius Intraspecific ×Pasinelli 2000
Passeriformes Meliphaga ssp. Interspecific ×Norman et al. 2007
Passeriformes Zonotrichia albicollis Intraspecific ×Formica et al. 2004
Passeriformes Certhia familiaris Intraspecific ×Aho et al. 1997
Mammals
Carnivora Lynx rufus Intraspecific ×McLean et al. 2005
Chiroptera Thre e species Interspecific × × Delaval et al. 2005
Primates Pygathrix nemaeus Intraspecific ×Workman and Covert 2005
Primates Callimico goeldii, Saguinus
labiatus, and S. fuscicollis
Interspecific ×Garber and Leigh 2001
Rodentia Apodemus argenteus
and A. speciosus
Interspecific ×Renaud and Millien 2001
Artiodactyla Odocoileus hemionus,
Cervus elaphus, and Bos taurus
Interspecific × × Stewart et al. 2003
Artiodactyla Cervus elaphus and
Odocoileus hemionus
Interspecific × × × Stewart et al. 2002, 2003
Artiodactyla Ourebia ourebi
and other ungulates
Interspecific ×Mduma and Sinclair 1994
Artiodactyla Fossil records of extinct
herbivore community
Interspecific ×MacFadden and
Higgins 2004
(Continued )
ap p e n d i x . Continued.
11_Baglione_08-146.indd 577 7/20/09 6:06:36 PM
578
—
Ba g l i o n e a n d Ca n e s t r a r i
—
au K , Vo l .
126
Orders and
families Species
Type of niche
partitioning
(intraspecific vs.
interpsecific)
Dimension of niche partitioning
ReferenceSpatial Temporal Diet
Feeding
behavior
Diprotodontia Macropus eugenii and
M. parma
Interspecific ×Lentle et al. 2003
Mixed assemblage
Araneae
(Lycosidae,
Salticidae)
and Coleoptera
(Carabidae)
Several species of Lycosidae,
Salticidae, and Carabidae
Interspecific ×Baldridge and Moran 2001
Fishes and
invertebrates
Sixteen fish species and four
invertebrate species
Interspecific × × Attrill and Power 2004
ap p e n d i x . Continued.
11_Baglione_08-146.indd 578 7/20/09 6:06:36 PM
