Raptor Nest Decorations Are a
Reliable Threat Against Conspecifics
F. Sergio,1*† J. Blas,1† G. Blanco,2 A. Tanferna,1 L. López,1 J. A. Lemus,1 F. Hiraldo1
Individual quality is often signaled by phenotypic flags, such as bright plumage patches in birds.
Extended phenotype signals can similarly show quality, but in these cases the signals are external
to the individual, often taking the form of objects scavenged from the environment. Through
multiple manipulative experiments, we showed that objects used for nest decoration by a territorial
raptor, the black kite (Milvus migrans), act as reliable threats to conspecifics, revealing the
viability, territory quality, and conflict dominance of the signaler. Our results suggest that animalbuilt structures may serve as signaling devices much more frequently than currently recognized.
nimals transfer information through anatomical, physical, and behavioral traits,
such as brightly colored body patches,
extravagant ornaments, or size-revealing calls
A
(1–3). Some species go to further extents by collecting objects to build external signaling structures or “extended phenotype signals” (4). Such
external signals may involve higher cognitive
abilities (5) and be subject to cultural transmission (6). Further, our ability to address questions
about such signals are facilitated by the facts that
(i) they are often flexible and less constrained
than bodily traits (4) and (ii) their constituent
materials may be readily available for experimental manipulation (7, 8). Despite the broader
appeal, extended phenotype signals have been
examined in only a handful of passerine bird
and fish species, and these were almost exclusively structures built solely for mate attraction
1
Department of Conservation Biology, Estación Biológica de
Doñana, Consejo Superior de Investigaciones Científicas (CSIC),
C/ Americo Vespucio, 41092 Seville, Spain. 2Department of Evolutionary Ecology, Museum of Natural Sciences, CSIC, C/ José
Gutiérrez Abascal 2, 28006 Madrid, Spain.
*To whom correspondence should be addressed. E-mail:
fsergio@ebd.csic.es
†These authors contributed equally to this work.
B
A
Fig. 1. Decoration of nests by black kites (Milvus migrans). (A) Highly decorated nest and (B)
selection of materials by kites relative to their availability in the environment. Kites show a preference
for white (c2 = 270.0, P < 0.0001) plastic (c2 = 57.0, P < 0.0001), whereas all other materials and
colors are used at rates equal to (other materials c2 = 0.1, P = 0.76) or less than (paper c2 = 68.1, P <
0.0001; cryptic colors c2 = 77.2, P < 0.0001; other colors c2 = 148.3, P < 0.0001) their availability
in the environment. [Photo credit: F. Sergio]
1
and courtship, such as the bowers of bowerbirds (5–8). However, several hundreds of species erect nest structures in manners that could
be compatible with extended phenotype signaling functions. Examples include the addition of man-made objects, stones, green plants,
snake skins, dung, or carnivore scats by passerines, storks, swans, penguins, corvids, raptors,
and fish and the building of multiple alternative
nests by wrens, weavers, and raptors (4, 9–14).
Therefore, although animals are thought to build
structures for communication only rarely (12),
nests could be signaling devices more frequently
than currently recognized.
We combined experimental manipulations and
long-term observations of a long-lived raptor to
show that nest decoration can act as an honest
threat to conspecifics, revealing the viability, territory quality, and conflict dominance of the signaler. Our model species, the black kite (Milvus
migrans), is a medium-sized migratory raptor. Pairs
occupy breeding territories that may vary markedly
in resource quality (15). Floating individuals are
prevented from breeding through social dominance
but may attempt violent territory takeovers, which
sometimes succeed (16) (fig. S1). Trespassing can
be frequent, especially in pre-incubation, and is
also aimed at stealing food resources obtained by
the residents. On return from migration after pair
formation, both partners contribute to nest building. One to 2 weeks before laying, they may both
place various man-made materials in the nest,
typically white plastic objects (Fig. 1A). The
objects seem placed so as to be highly visible and
are collected during the peak period of territory
trespassing and long after pair formation. Thus, we
hypothesized that they serve as an extended phenotype signal of threat against intruders (table S1).
We used a well-studied (15, 16) (fig. S2)
population of marked, known-age (1 to 25 years
old) kites in Doñana National Park. To investigate
the signaling function of nest decorations (17), we (i)
assessed decoration levels at 127 nests built by
individuals of known age and body size, which
were subsequently intensively monitored to estimate their viability (here defined by subsequent
survival and offspring production); (ii) compared
nest decorations with objects available in the
environment; (iii) offered objects to marked individuals to examine their propensity to use decorations; (iv) estimated trespass rates and aggression
of intruders for both nonexperimental and experimental pairs (i.e., those whose nest decorations
had been augmented); (v) tested whether nest
decorations predicted the efficiency of resource
monopolization mediated by aggression within a
Fig. 2. Change in mean (T 1 SE) nest
decoration by black kites (black line)
with age (n = 127). Placement of freely
available items (gray) was highest for
birds in prime age (7 to 12 years old)
and lowest for young and old individuals (n = 49).
competitive feeding environment away from the
nest; and (vi) examined the egg predation rates of
experimental dummy kite nests with and without
decorations. Through this series of experiments,
we specifically tested for the presence of an honest extended signal by addressing four hypotheses, as proposed by Searcy and Nowicki (3): (i) is
the signal reliable; (ii) do receivers respond to the
signal in a way that benefits signalers; (iii) is the
signal costly, and is the cost higher for lowerquality individuals; and (iv) is there deceit (17)
(table S1)?
Nest decorations were observed in 77% of the
nests (n = 127), appeared in the last 20 days
before laying, and declined slightly during the
incubation period and markedly thereafter (fig.
S3). Both sexes were equally likely to carry
decorations (males 15 times, females 12; binomial test, P = 0.70). When compared to availability in transects (Fig. 1B), kites overselected
plastic materials (c2 = 57.0, P < 0.0001) and
white color (as assessed by human vision; c2 =
270.0, P < 0.0001). All other materials and colors
were avoided or used according to availability
(Fig. 1B). When birds were offered a set of experimental objects in equal availability (17), 29
of 33 pairs that collected objects placed only
white plastic items in their nest, two collected
both white and transparent items, and another
two collected both white and green items. White
was overselected ( c2 = 100.7, P < 0.0001), and
the other colors were avoided (green and transparent c2 = 24.5, P < 0.0001).
Is the signal reliable (hypothesis i)? Nest decoration increased with territory quality and body
condition and exhibited a quadratic (parabolic)
relationship with age (table S2 and Figs. 2 and 3):
The level of decoration increased up to ages 10 to
12 and declined thereafter with senescence (Figs. 2
and 3). Similarly, 37% of the pairs refrained from
collecting any offered item despite its prolonged
availability. These animals had lower-quality territories and differed in age from individuals that
used the offered items (table S3): Individuals that
refrained from signaling were very young or very
old, whereas those that used the decorations to
signal were predominantly in prime age (7 to 12
Fig. 3. Change in level of nest decoration in black kites. Level of decoration was (A) lowest for young birds, (B) increased up to ages 10 to 12 years old, and
(C) declined thereafter with senescence. [Photo credit: F. Sergio]
years old; Fig. 2). The rate and success of attacks on
trespassers increased with decoration levels (table
S4). Similarly, in feeding observations, the percent
of time an individual spent eating and its success
rate in food-related aggressive interactions were
related to its nest decoration level (table S5).
Do receivers respond to the signal and do they
respond in a way that benefits signalers (hypothesis
ii)? In pairs without experimental nest augmentation, territory intrusion rates were lower for highly
decorated nests (table S4), consistent with the
hypothesis that trespassers avoid decorated nests.
However, intruder pressure actually increased when
we experimentally augmented the decorations
(table S6). This suggests that nonterritorial animals
or “f loaters” may be stimulated to attack pairs that
suddenly advertise a high-quality territory.
Higher levels of nest decoration predicted
higher subsequent breeding success and survival
(table S7 and Fig. 4), suggesting that birds may
benefit from lower rates of risky fights associated
with higher-quality advertisement.
Is the signal costly, and is the cost higher for
lower quality individuals (hypothesis iii)? Predation rates of experimental eggs were higher for
decorated dummy nests (81.3% predated, n =
16) than for nondecorated dummy nests (31.3%,
n = 16, c2 = 8.54, P = 0.003), indicating that there
Fig. 4. Nest decoration by
black kites increased with
the viability of the signaler,
as estimated by breeding
performance (number of fledglings produced, black circles,
n = 127) and survival until
spring (white squares, n = 76).
Data are mean T 1 SE.
Fig. 5. Experimental augmentation
of nest decoration. Mean (T 1 SE)
attack rates of black kites on trespassers were higher in prime age
(7 to 12 years old; black circles, n = 25)
individuals and lower in young or
old (≤6 or ≥13 years old; white
squares, n = 40) animals.
is a cost to advertising quality through nest
decoration. Similarly, trespassing rates increased
for all individuals in the augmentation experiment, but only those in prime age managed to
increase their attack rate in response (table S6 and
Fig. 5). Very young or senescent individuals appeared incapable to counteract the cost of signaling (Fig. 5); thus, it appears this cost is higher
for lower-quality individuals.
Is there deceit (hypothesis iv)? In the equal
availability experiment, lower-quality individuals
almost systematically refrained from signaling
(Fig. 2). One week after the augmentation experiment, 85% of the individuals in prime age
had retained the plastic we placed in their nest,
whereas 87% in the other age classes had
removed it. Age and its quadratic effect were
the only predictors of the likelihood that a pair
would retain or expel the experimental plastic
(table S8). Deceit, if present, seems rare.
Our results show that nest decoration is a
graduated signal that conveys complex information on territory quality, individual viability, and
dominance in social interactions. We found no
support for alternative hypotheses (tables S1 and
S9). Reliability of the signal was reinforced because lower-quality individuals refrained from
dishonest signaling, even though such cheating
would have been possible. Theoretical studies
predict signaling abstention by lower-quality individuals in the presence of agonistic retaliatory
costs imposed by receivers (18). Such social costs
were evident in this study: Advertisement of highquality resources was met with aggressive challenges. The costs of such challenges could be
disproportionately high for cheating individuals,
because advertising high-quality resources may
attract strong contestants (19) that are able to
displace dishonest signalers through aggressive, and physically damaging, conflicts (16)
(fig. S1). Consistent with such disproportional
costs, only individuals in prime age were able
to respond to the increase in challenges stimulated by experimental nest augmentation. Lowerquality individuals were not able to match their
defense rates to the cheating decoration levels
that we imposed. Social punishment has been
recurrently shown as a major theoretical determinant of communication honesty, especially for
signals involving minimum production costs
[e.g., (20, 21), review in (2)], such as many
extended phenotype signals. This may explain
why social punishment and cheating abstention seem common in such communication systems [e.g., (7, 22–26)].
Extended phenotype signals can be reliable
indicators of both individual and territory quality. Previous analyses have shown that levels of
external signals may increase from juvenile to
adult age classes [e.g., (23, 27)] or be individually repeatable through time [e.g., (28, 29)].
Our findings confirm such earlier studies and
expand them by showing a clear senescent decline in signaling strength. This reinforces the idea
of individuals signaling their physical prowess,
which increases and then declines with age. Further, our findings indicate that external signals can
be used in the context of resource defense and do
not solely signal reproductive quality in a sexual
selection context, although reinforcement of pair
bonding may have contributed to our results (10).
In line with these ideas, many characteristics typical of the objects used to create extended phenotype signaling structures make them optimal as
signals of territorial defense: high visibility, effectiveness in the absence of the signaler, encoding of social dominance and motivation, ease
of deconstruction, and reliability enforced by
punishment of cheaters [reviews in (1–4)].
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30. We thank F. J. Chicano, J. Giralt, and F. G. Vilches for
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reviewers greatly improved a previous draft of the
manuscript. The study was funded by the research
projects CGL2008-01781, JA-58, RNM 1790, and RNM
03822 granted by the Junta de Andalucía, Ministerio de
Ciencia e Innovación, and Natural Research Limited.
Supporting Online Material
www.sciencemag.org/cgi/content/full/331/6015/327/DC1
Materials and Methods
Figs. S1 to S3
Tables S1 to S9
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1b
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