Jose A. Donazar Alejandro Travaini Olga Ceballos
Alejandro Rodriguez Miguel Delibes Fernando Hiraldo
Effects of sex-associated competitive asymmetries on foraging group
structure and despotic distribution in Andean condors
Abstract Phenotype-limited interference models assume
competitive asymmetries among conspecifics and unequal sharing of resources. Their main prediction is a
correlation between dominance status and patch quality:
dominant individuals should preferentially exploit better-quality habitats. We tested assumptions and predictions of the phenotype-limited interference model in
Andean condors (Vultur gryphus), a New World vulture
with strong sexual size dimorphism (males are 30—40%
heavier than females). We recorded searching birds in
habitats differing in quality: mountains and plains. We
also observed scavenging behaviour at 20 sheep carcasses, and videotaped 5 of them. Intraspecific hierarchy
at carcasses was based on size: males dominated females
and, within each sex, older birds dominated younger
ones. Adult males and juvenile females occupied extreme
positions in the feeding hierarchy. Aggression was directed at those individuals belonging to lower hierarchical levels. In high-quality areas (mountains), more
condors arrived at carcasses. Juvenile females were more
often observed searching in low-quality areas (plains),
far from breeding areas and main roost sites. GLM
analyses of individual behaviour showed that the hierarchy did not influence time of arrival, but low-ranking
individuals spent more time at carcasses, especially if the
number of condors at arrival was high. Additionally,
low-ranking condors spent less time feeding at carcasses
J.A. Donazar ()) A. Travaini 1 A. Rodriguez
M. Delibes F. Hiraldo
Department of Applied Biology
Estacion Biologica de Donana (C.S.I.C.), Avda. Ma Luisa s.n.
E-41013 Sevilla, Spain
e-mail: Donazar@ebd03.ebd.csic.es, Tel.: +34-95-4232340
Fax: +34-95-4621125
O. Ceballos
Grupo de Estudios Biologicos Ugarra, Carlos III 19 40 I,
E-31002 Pamplona, Spain
Present address:
1
Centro de Investigaciones de Puerto Deseado, Universidad
Nacional de la Patagonia Austral, Almirante Brown y
Colon s/n, Puerto Deseado 9050, St. Cruz, Argentina
when individuals of higher hierarchical levels were
present. On the other hand, the number of condors
present had a positive effect on feeding rates of dominant individuals, probably because of a reduction in
individual vigilance. These results support most of the
assumptions and predictions of the phenotype-limited
distribution model, although a spatial truncated distribution between phenotypes was not observed. Asymmetric feeding pay-off, unequal parental roles and sexual
selection constraints could favour sexual divergence in
body size in Andean condors.
Key words Competitive asymmetries Despotic
distribution Foraging behaviour Vultur gryphus
Introduction
Cooperation in searching for and manipulating food has
evolved many times within vertebrates (Wilson 1975).
Individual advantages of foraging in groups are related
to the increased probability of detecting food, since the
area surveyed by groups is larger than that covered by a
single animal, and individuals have the opportunity to
observe other conspecifics feeding or displaying behaviours related to feeding (Ward and Zahavi 1973; Krebs
1974; Caraco 1981; Pulliam and Caraco 1984; Clark and
Mangel 1986; Huntingford and Turner 1987; Benkman
1988). Moreover, when food items are large in size, food
manipulation (killing, dismembering and defence against
interspecific competitors) can be better achieved among
conspecifics than by single individuals (Schaller 1972).
Finally, foraging in groups increases the probability of
predator detection and avoidance (Gluck 1986; Lima
and Dill 1990). On the other hand, the main costs of
group foraging have usually been related to decreased
food intake per individual as group size increases (Vickery et al. 1991).
Different patterns of food sharing among conspecifics
have been proposed. The ideal-free distribution model
(Fretwell and Lucas 1970; Fretwell 1972) assumes that
56
individuals have similar competitive abilities and move
freely among patches in relation to the reward expected
for each of them. Consequently, better patches will receive more individuals but the reward would be similar
in each visited food site. Phenotype-limited models
consider the role of unequal competitive abilities
(asymmetries) among individuals (Parker and Sutherland 1986; Milinski 1988; Milinski and Parker 1991;
Lindstrom and Ranta 1993). The asymmetries are
mainly based on age and body size differences: larger
and older individuals dominate in interactions at feeding
grounds (Bautista et al. 1995). Competence asymmetries
among individuals could have important effects on
group structure, rate of food intake and individual
spatial distribution in social foraging species (see among
others Parker and Sutherland 1986; Milinski 1988;
Milinski and Parker 1991; Rita et al. 1996).
Studies testing interference models are scarce (but see
Monaghan 1980; Goss-Custard et al. 1984; Bautista et al.
1995; Milinski et al. 1995). Among vertebrates, vultures
are excellent candidates for studying the social foraging
implications of despotic competence (Kirk and Gosler
1994). They exploit animal carcasses, an unpredictable
and ephemeral resource; carcasses are located through
processes such as information transfer at information
centres and local enhancement (Buckley 1996). Individual foragers gather at feeding grounds and strong intraspecific competition arises (Mundy 1982; Wallace and
Temple 1987). Morphological constraints and k-related
life history traits make vultures appropriate subjects to
compare competitive asymmetries related to age since
many species experience long periods before sexual
maturity. In addition, although intraspecific variation in
body size is rare among vultures it can be found among
the subspecies coexisting in wintering quarters (Kirk and
Houston 1995) or between sexes in the Andean condor
Vultur gryphus) (Del Hoyo et al. 1994).
The objectives of this paper were as follows. (1) To
test the existence of intraspecific competitive asymmetries in Andean condors during scavenging activities. In
this species, males weigh 36—37% more than females
(11—15 kg vs 8—11 kg; Del Hoyo et al. 1994), and sexual
maturity is reached after 6 years of age (Del Hoyo et al.
1994), which can lead to strong intraspecific feeding hierarchies. (2) To study the effects of competitive asymmetries on social foraging strategies, focusing on
foraging group structure and foraging rewards. We tested the phenotype-limited interference model (Sutherland and Parker 1985; Ranta et al. 1993; Rita et al.
1996). Model assumptions are that phenotypes differ in
dominance status, that pay-off for subordinates decreases when the number of dominants increase, and
that relative pay-offs of phenotypes change between
patches. The main prediction is a correlation between
dominance status and patch quality, with stable and
truncated distributions of phenotypes between patches
(dominants would be concentrated exclusively in patches
of higher quality). Foraging activities were studied in
two areas of different quality: mountains (high) and
plains (low). In addition, comparisons were made in a
single habitat (mountain) during two seasons with different foraging quality: spring (low) and summer (high).
Methods
Study area and sites
This study was conducted in the Neuquen Province, northern Argentinean Patagonia, in an area with a radius of 60—70 km centred
in Junin de los Andes (39057’S and 71005’W, 780 m a.s.l.). The
weather is cold and dry with a pronounced gradient of rainfall from
800 mm average annually in the mountains to 300 mm on the
eastern steppes. The region belongs to the Patagonian phytogeographic province, Western District (Cabrera 1976). The Andean
condor, once widely distributed along the Cordilleran Range from
Venezuela to Tierra del Fuego, is now rare in most of its range but
still relatively abundant in the study area (Del Hoyo et al. 1994).
Two zones with different quality of foraging habitats were
considered for our study. The criteria for quality were: (1) the
distance to Andean condor breeding and roost sites and (2) the
possibility to safely exploit the carcasses. Condors are birds at the
limit of flight capacity due to their high wing loading (McGahan
1973). Large adult males experience difficulties taking off after
feeding (Palermo 1983); occasionally, birds have to climb steep
slopes on foot until they are high enough to fly (personal observations). Hence, flat areas are risky for condors since the probability of predation increases. Carnivores have been seen to kill
vultures feeding at carrion (Donazar and Ceballos 1988; Mundy et
al. 1992) and the capture or killing of scavenging condors by humans is (or has been) not rare (McGahan 1972; Palermo 1983).
Carcass availability is not a primary component of habitat
quality since carrion abundance does not vary within our study
area. Sheep carcasses are the main food resource for condors in the
study area (72.1% of appearances, n = 179 pellets, personal observation). Availability of sheep carcasses is very high throughout
the whole study area where tens of thousands of sheep head are
raised annually (personal observation).
We considered two different quality areas.
High quality (mountain areas)
The mountains (spurs of the Andean range) occupy the northern
and western portions of the study area, with the highest peaks
reaching 3600 m. Condor roosts and breeding areas are between
1190 and 2000 m a.s.l. (personal observation). Human disturbance
is very low: there are some isolated human settlements and a few
non-paved roads. Information from sheep farmers suggests that
carcass availability is similar in spring and summer. Flight conditions for foraging condors, however, should be much better in the
summer due to warmer weather and thermal formation (Pennycuick 1972); consequently, the probability of gaining carcasses
(quality of the habitat) would increase during the summer.
Low quality (plains)
The plains are located in the south-eastern part of the study area at
500—700 m a.s.l., and are dissected by steep valleys. There is a single
condor roost site on an isolated hill at 1000 m a.s.l. which is regularly visited by the birds. The human population is larger than in
the mountains: there is a paved road and a town with 5000 inhabitants (Junin de los Andes).
Foraging behaviour
To study the foraging behaviour of Andean condors, we placed
sheep carcasses both in a mountain area (Puerto de Pilolil, 1160 m
57
a.s.l.), and in a plain zone (Mendana hills, 840 m a.s.l.). Observations were made between 10 November—20 December (spring) of
1991 and 1992, and between 12 January—10 February (summer) of
1995. To establish the existence of competitive asymmetries, three
age classes were considered: juvenile, subadult and adult condors.
Adult birds have black plumage with white secondaries and upperwing coverts, and a conspicuous white neck ruff. Juveniles are
dull brown (Del Hoyo et al. 1994). Subadult birds look like adults
but their secondaries and upperwing coverts are in ochre or grey
shades, never pure white. Males were distinguished from females
mainly by the presence of a comb of variable size. Unlike Wallace
and Temple (1987), we did not attempt to distinguish more age
categories: according to our field experience, it is extremely difficult
to detect less showy characters (such as iris colour) from several
hundred metres away, and impossible to determine accurately the
age of each individual when numerous condors gather at carrion,
with the birds constantly shifting position.
The data recorded in the course of 309 h of systematic observations during spring (66 in the mountains and 243 on the plains)
were used to obtain information on the age and sex of the birds that
were exploring the ground. Both age class and sex of all the flying
condors observed while travelling in the study area during the
whole study period were also recorded. Subadults were pooled with
juveniles, since assessing characters such as a white neck ruff in
flying birds at medium or long distances is difficult. Most of the
birds were observed during the spring (n = 56 in the mountains
and n = 61 on the plains), while 12 and 17 birds were observed in
the summer season in the mountains and on the plains, respectively.
The samples of the two periods did not show significant differences
in relation to age and sex frequencies (N x M tests, P > 0.05), so
we pooled data from spring and summer for further analyses.
Condor scavenging behaviour was studied by observing 18
sheep carcasses, 7 placed in the mountain area and 11 on the plains
site during the spring season. Two people watched simultaneously,
with telescopes, from a car or hides at a minimum of 300 m away
from the carcasses, not interfering with the behaviour of the birds.
We recorded the age class, the sex, the arrival and departure times
for every individual, and all the interactions among individuals,
identifying the age and sex of actors and receivers and whether or
not the displacement attempt was successful.
We also examined 14 h of video film of five sheep carcasses in
the mountain area during the summer (January and February 1995)
and one carcass on the plain during the spring (December 1992).
We recorded: (a) all condor arrivals and departures until the carcasses were fully consumed by the condors or any other avian
scavenger species; (b) the total time that every individual spent in
feeding activities: every 10 s we recorded if the individual was (1)
feeding: i.e. pecking the carcass or with its head towards the carcass
below the horizontal level, (2) watching: the condor was less than
1 m away from the carcass, with its head erect above the horizontal
level, (3) out: the condor was more than 1 m away from the carrion.
Data analysis
Determination of feeding hierarchies, and the comparisons between
frequencies of condors scavenging in the three studied zones and
between scavenging and searching condors were performed
through univariate analyses following Wells and King (1980) and
Siegel and Castellan (1988). Hierarchies among sex and age categories were studied, on the basis of the observed interactions
among the individuals sharing the carcasses, following similar
studies on scavenging birds (Alvarez et al. 1976; Wallace and
Temple 1987; Hiraldo et al. 1991; Kirk and Houston 1995). For
each category we calculated the percentage of aggressive actions
performed and won against the other categories. To determine the
existence of dominance we compared this frequency with that expected by chance (goodness-of-fit test); one-tailed x2 and Fisher
exact tests were employed following Senar et al. (1989).
Directionality was studied in the same data. As pseudoreplication is a common problem in studies based on unmarked individuals (Kirk and Houston 1995), we tried to reduce the variance
due to individual differences using the filmed carcasses and taking
into account the interactions directed for each individual separately. For each bird we obtained one index for each age-sex category with which it interacted. The index checked if the rate of
aggression performed by the bird towards individuals of each category was different to those expected by chance. The index was
calculated as (number of aggressions directed to category A/total
number of aggressions performed)/(number of condors belonging
to category A/total number of condors). Index values above 1
represent frequencies of aggression above those expected. When
only birds of two age-sex categories were present we did not perform calculations, as the potential aggressor had no choice.
The analyses of arrival time, time spent at carcasses and time
spent feeding were performed through generalized linear models
(GLMs; Nelder and Wedderburn 1972; Dobson 1983; McCullagh
and Nelder 1983). It allows us to determine a wide range of relationship between the response and explanatory variables and the
use of different error formulations according to data characteristics. We fitted each explanatory variable to the observed data following a modification of the traditional forward stepwise procedure
which conducts, through the principle of parsimony, the most
minimal adequate model able to describe the data set (Donazar
et al. 1993; Bustamante et al. 1997). If a preliminary exploratory
analysis suggested a curved response we fitted a quadratic function
and a cubic term to improve the model. We also tested square root
and logarithmic transformations if the data suggested multiplicative effects. Model criticism was made following Crawley (1993).
We characterized each of the response variables as follows. The
arrival time was calculated for each condor as the difference (in
minutes) between its arrival and that of the first condor. These
values were log-transformed and a GLM model with an identity
link and assuming normal error was fitted (equivalent to a multiple
linear regression). Time spent by individual condors at carcasses
was measured in minutes and log-transformed. Finally, the time
that the condors spent feeding was calculated by examining the
filmed carcasses. The variable was the frequency of 10-s sequences
in which the bird was observed feeding. We considered a binomial
distribution of errors (denominator = 1) and used a logistic link
(equivalent to a logistic regression).
The explanatory variables were characterized as follows:
(1) Hierarchy: following our results (see below), four categories
were considered, from the first dominant to the last subordinate
— adult male, juvenile male, adult female, juvenile female.
(2) Carcass: each carrion was considered as a different sample.
(3) Zone (habitat quality): following the considerations for seasonal, physiographic and food availability conditions we determined three factors — mountain in spring, mountain in
summer and plain in spring.
(4) Number of condors present when each individual arrived.
(5) Number of condors of higher hierarchical level present when
each individual arrived.
(6) Presence or absence of individuals of higher hierarchical levels.
(7) Maximum number of condors simultaneously present during
the time that each individual spent at the carcass.
(8) Maximum number of condors of higher hierarchical levels simultaneously present during the time spent by the individual at
the carcass.
By considering the above variables, through GLM models we
minimized the pseudorreplication problem linked to the similarity
of conditions taking place at each carcass and day, introducing as
factors both the carcass and habitat quality variable (zone).
Results
Numbers of condors and foraging habitat selection
During the 66 h of systematic observation in mountain
zones, a total of 33 searching condors (0.50 individuals/h)
58
were detected, while during the 243 h of observation on
the plain, 51 condors were detected (0.21 individuals/h).
A further 51 condors were observed in a non-systematic
way. Altogether, we accurately determined the sex and
age of 117 birds. In the mountains, 56 searching individuals were observed, of which 21 (37.5%) were adult
males, 5 (8.9%) adult females, 19 (33.9%) young males,
and 11 (19.6%) young females. On the plain, 61 condors
were observed, of which 15 (24.5%) were adult males, 4
(6.6%) adult females, 13 (21.3%) young males, and 29
(47.5%) young females. The comparison of frequencies
of each sex and age category observed in both habitats
showed significant differences (N x M exact test,
P = 0.002). The partitioning of the contingency table
revealed that there were no significant differences between the frequencies of male adults and male juveniles
(x2 = 0.007, P > 0.9) and between males (adults plus
juveniles) and adult females (x2 = 0.034, P > 0.8);
however, there were differences between juvenile females
and the remaining categories (x2 = 10.100, P < 0.01).
In spring and in the mountains a total of 158 condors
were observed to land and feed on all 7 sheep carcasses.
The total number of landing birds ranged between 5—38
(mean = 20.6, SD = 12.8): 79 (50.0%) were adult
males, 13 (8.2%) adult females, 29 (18.3%) young males
and 37 (23.4%) young females. The maximum number of
simultaneously observed condors ranged between 2—18
(mean = 7.2, SD = 5.2). On the plain, 54 condors arrived at 8 (72.7%) of the 11 monitored sheep carcasses.
The total number of landing birds ranged between 2—16
(mean = 7.1, SD = 5.3). An additional 12 scavenging
condors were also observed at non-focal carcasses found
during this study. In total, of the 66 observed individuals,
18 were adult males (27.3%), 12 adult females (18.2%),
15 (22.7%) young males and 21 (31.8%) young females.
The maximum number of simultaneously observed condors ranged between 1—5 (mean = 2.6, SD = 1.5).
During the summer and in the mountains, we observed
a total of 35 condors at the 5 sheep carcasses
(mean = 7.0, SD = 5.4, range: 1—14); 8 (22.9%) were
adult males, 11 (31.4%) adult females, 6 (17.1%) young
males and 10 (28.6%) young females. The maximum
number of simultaneously observed birds at a carcass
ranged between 1—6 (mean = 3.2, SD = 1.9).
Application of statistical comparisons to the above
data revealed that, in spring, significantly more condors
landed at carcasses in the mountains than on the plain
(Mann-Whitney U-tests, Z = 7.0, P = 0.026); in addition, more condors landed in the mountains in the spring
than in the summer, (Z = 5.0, P = 0.048). The same
trends were observed regarding the maximum number of
condors present at carcasses: spring mountain versus
spring plain (Z = 4.5, P = 0.007), spring mountain
versus summer mountain (Z = 3.5, P = 0.018). Finally,
by comparing sex and age frequencies of searching birds
with those of feeding condors (see above and Fig. 1), no
significant differences were detected within the mountains
(x2 = 6.426, df = 3, P = 0.0926) or plain x2 = 5.507,
df = 3, P = 0.1382).
It was notable that the male/female proportion in
searching birds seen in the mountains during the spring
differed markedly from 1:1 for adult birds (21 males/5
females, binomial test, P = 0.004), but not for juveniles
(19/11, P = 0.204). The same trend was detected in
birds landing at carrion: adults (80/13, P = 0.0001),
juveniles (29/37, P = 0.390). On the plain, the trends
were similar: searching birds — adults 15/4 (P = 0.020),
juveniles 13/29 (P = 0.192); scavenging birds — adults
18/12 (P = 0.363), juveniles 15/21 (P = 0.406). In
contrast, during the summer and in the mountains, the
proportion of sexes did not differ from 1:1 either in
landing adults (8/11, P = 0.648) or juveniles (6/10,
P = 0.454). This means that the fraction of adult females increased from spring to summer in birds scavenging in mountain areas (N x M exact test, P =
0.00013).
Competitive ability according to sex and age
The results obtained from all the interactions showed the
existence of a distinct hierarchy (Fig. 2). Adult males
directed and won aggressions against all other age and
sex classes; subadult males dominated juvenile males,
adult females and juvenile females (no simultaneous
meetings between subadult males and subadult females
took place); juvenile males dominated females of all age
categories; adult females dominated over subadult and
juvenile females; subadult females dominated over juvenile females, while juvenile females did not dominate
any other age category. Males clearly dominated females, independent of age, and within each sex group,
older birds were dominants.
Regarding directionality, it could be observed
(Fig. 3) that adult males attacked the subordinate categories with a similar frequency (Kruskall-Wallis test,
KW = 3.073, P = 0.238). In contrast, adult and juvenile females directed their attacks significantly more
to juvenile females (KW = 7.200, P = 0.006, and
KW = 13.524, P = 0.000, respectively). These results
clearly indicate that condors direct their aggression to
those individuals of lower hierarchy, except, clearly,
those at the end of the hierarchical scale (juvenile females) which only attack individuals of their own category. When we investigated if the rate of aggression
(numbers/minute) received by an individual condor of
low-ranking categories (females) depended of the number of dominant individuals present, we did not find any
significant correlation, and the trends were contradictory: adult females (rs = 0.387, P = 0.327, n = 8),
juvenile females (rs = —0.313, P = 0.321, n = 12).
Data recorded for juvenile males were too low to conduct a similar analysis.
The GLM model on individual arrival time accounted for the 36.3% of the initial deviance, and did
not show data overdispersion. Only two variables were
included into the model: carcass (70.7% of the explained
deviance) and number of condors at arrival (29.3%)
59
Fig. 1 Percentage of condors
that were observed searching
for and feeding at carrion in
mountain and plain areas during spring (AM adult males, JM
juvenile males, AF adult females, JF juvenile females)
(Table 1). This indicates that time of arrival is highly
variable between carcasses and late-arriving individuals
encountered a higher number of condors. Number of
condors of higher hierarchical level entered initially into
the model but its effect disappeared when the number of
condors was included.
The GLM model dealing with the time spent by individual condors at carcasses accounted for 66.2% of the
original deviance and did not show data overdispersion.
Variables included were carcass (66.2% of the explained
deviance), number of condors at arrival (24.3%), and
hierarchy (12.8%) (Table 2). These results indicate that
time spent by individual birds was mainly related to the
particular characteristics of each carcass. Additionally,
within each carcass, the hierarchy had an important influence: dominant individuals (adult males) spent the
minimum time at carcasses whereas juvenile females
stayed there longer (Fig. 4). Juvenile males and adult
females showed a similar trend, intermediate between
the two extreme hierarchies. The differences among hierarchies increased when the number of condors present
rose; thus, subordinate individuals (juvenile females)
were very sensitive and the time they spent at carcasses
increased more sharply than in the other categories.
The best model obtained for time spent feeding by
individual condors accounted for 25.7% of the initial
deviance and did not show data overdispersion
(Table 3). It included four variables: carcass (28.4% of
the explained deviance), hierarchy (14.6%), presence/
absence of condors of higher hierarchy (10.2%), and
maximum number of condors during the individual stay
(7.2%). Additionally, we found a significant interaction
60
Fig. 2 Number of displacement
attempts at carcasses recorded
among condors of each age and
sex category [x-axis target (receiver) individuals: AM adult
males, SBM subadult males,
JM juvenile males, AF adult
females, SBF subadult females,
JF juvenile females). For each
bar, successful attempts are in
black and unsuccessful ones in
white. Note the different y-axis
scales for adult males and the
other categories. Significance of
one-tailed chi-square and Fisher exact tests are shown above
bars ( P < 0.05, P < 0.01,
P < 0.001, n.s. not significant; samples with n < 4 were
not considered for statistical
tests)
between hierarchy and maximum number of condors
(14.6% of the explained deviance). The representation of
the predicted feeding probabilities for a given carcass
(the first factor included in the analysis) showed that
dominant condors spent more time feeding than subordinates. The hierarchical differences were more acute
when the number of condors present was high and when
there were individuals of higher hierarchical levels
(Fig. 5). It is worth noting that subordinate individuals
such as juvenile females spent more time feeding than
more dominant birds when the number of condors and
competitors was very low.
61
Table 2 GLM model for time spent at carcasses by individual
condors (log-transformed), using normal error and identity link.
The values for the explanatory variable carcassss (factor levels = 20) are not shown
Parameter
estimate
Constant
Juvenile males
Adult females
Juvenile females
Number of condors at
arrival
Residual deviance
df
—2.030
0.418
0.200
0.413
0.073
SE
0.219
0.151
0.163
0.140
0.014
112.2
200
When the condors stopped feeding they abandoned
the carcass but remained nearby. This was shown by
significant correlations detected between the frequency
of feeding and time spent away from the carcasses (adult
males: rs = —0.783, P = 0.003, n = 12; juvenile males:
rs = —0.476, P = 0.243, n = 8; adult females:
rs = —0.563, P = 0.036, n = 14; juvenile females:
rs = —0.685, P = 0.014, n = 12). On the other hand,
when we correlated the frequency of feeding and time
spent in vigilance attitudes (watching over) we found a
significant trend only for adult females (adult males:
rs = 0.007, P = 0.983, n = 12; juvenile males:
rs = —0.048, P = 0.935, n = 8; adult
females:
rs = —0.644, P = 0.013, n = 14; juvenile females:
rs = 0.172, P = 0.594, n = 12).
Discussion
Dominance patterns
Our results showed clear individual differences in competitive ability, which is a primary assumption of pheFig. 3 Directionality of aggressions performed by individual condors.
The index (y-axis) represents the value (mean ± SD) of a fraction
which evaluated the observed rate of aggressions with respect to the
total number of potential receptors (AM adult males, JM juvenile
males, AF adult females, JF juvenile females). Index values above 1
represent frequencies of aggressions above those expected. Sample
sizes are shown above and below bars
Table 1 GLM model for time of arrival at carcasses of individual
condors (log-transformed), using normal error and identity link.
The values for the explanatory variable carcassss (factor levels = 17) are not shown
Parameter
estimate
Constant
Log (number of condors
at arrival + 1)
Residual deviance
df
2.271
0.747
283.8
195
SE
0.461
0.131
Fig. 4 Time spent at carcasses by individual condors as predicted by a
GLM with normal error and identity link. Explanatory variables are
hierarchy and number of condors at arrival (AM adult males, JM
juvenile males, AF adult females, JF juvenile females)
62
Table 3 GLM model for time feeding at carcasses by individual
condors in relation to the total time of observation, using binomial
error (denominator = 1) and logistic link. The values for the explanatory variable carcassss (factor levels = 5) are not shown
Parameter
estimate
Constant
Juvenile males
Adult females
Juvenile females
No competitors
Maximum number
of condors
Hierarchy x maximum
number of condors
Residual deviance
df
SE
1.173
—0.380
—0.231
0.439
0.685
1.078
0.133
0.127
0.107
0.263
0.110
0.219
—0.259
0.070
735.4
35
notype-limited models (Parker and Sutherland 1986).
Intraspecific hierarchy at carcasses is based on size:
Fig. 5 Frequency of time spent
feeding by individual condors
as predicted by a GLM with
binomial error and logistic link.
Explanatory variables are hierarchy, maximum number of
condors present during the time
spent by the individual at the
carcass, and presence/absence
of competitors (AM adult
males, JM juvenile males, AF
adult females, JF juvenile females)
larger males were dominant over the smaller females.
The effect of age was apparent only within each sex:
older birds dominate younger birds. The analyses of
interaction directionality and intensity of supplantation
attempts revealed that interactions were preferentially
directed at lower-ranked individuals within the feeding
hierarchy. Very few interactions were aimed at adult
males, and when they did occur they came from other
males. This hierarchical pattern partially differs from
that described by Wallace and Temple (1987) when
studying intraspecific condor fighting in Peru. They
stated that, on occasion, age could be an important
component in hierarchy settlement — a female could
dominate a male more than one year her junior. Our
findings agree more with studies where the supplanting
behaviour in carrion-eating bird species showing sexual
dimorphism is related to intraspecific hierarchies defined
by body size (Knight and Knight 1988; Garcelon 1990;
Hiraldo et al. 1991, Kirk and Houston 1995). In nondimorphic vulture species, intraspecific hierarchy seems
63
to be determined by age and some behavioural factors dominant individuals (i.e. adult males) is higher in the
such as hunger (Koford 1953; Anderson and Horwitz mountains (better-quality area). From the results ob1979; Mundy 1982; Elosegi 1989).
tained modelling the feeding-rate intake, we could reasonably expect a reduction in the relative pay-offs for
subordinate birds (mainly juvenile females) in these
Hierarchy and foraging pay-offs
zones. Increasing interference in larger conspecific
groups and subsequent reduction of food intake by
The first assumption of phenotype-limited models is that subordinate individuals has been observed in other sopay-offs for subordinates decrease when the number of cial-foraging species such as turkey vultures (Cathartes
dominant condors increases. Our results support this, aura, Kirk and Houston 1995), herring gulls (Larus ar
since subordinate individuals obtained less food in the gentatus, Monaghan 1980; Monaghan et al. 1986), oyspresence of dominant birds, as has been observed in tercatchers (Haematopus ostralegus, Goss-Custard et al.
many other social-foraging species (see among others: 1984), and mute swans (Cygnus olor, Milinski et al.
Baker et al. 1981; Heinrich 1988, 1994; Senar et al. 1989; 1995).
Senar 1994; Kirk and Houston 1995 and references
therein). In our case, however, and contrary to the observations of other authors (Balph 1977; Bekoff and Habitat segregation
Scott 1989), we did not find a direct relationship between
the number of competitors and the frequency of ag- The main prediction of the phenotype-limited model is a
gression directed to subordinate birds. This seems to be positive relationship between dominance status and
due to the fact that when competitors are present, ex- patch quality. Our results support the idea that despotic
tremely subordinate condors, especially juvenile females, competence determines patch segregation in the studied
remain at the edge of the scavenging group and avoid region. Extreme dominants (adult males) search for food
becoming involved in aggressive encounters (see also and scavenge mainly in high-quality areas (mountain)
Alonso et al. 1997). In fact, our results show that time whereas extreme subordinates (juvenile females) forage
spent feeding and time spent away from the carcass are mainly on the plains. Similar segregation patterns have
inversely correlated. This may also explain why subor- been described for other socially foraging species (Modinates tended to spend more time at carcasses when the naghan 1980; Goos-Custard et al. 1984; Bautista et al.
number of condors present was high, whereas more 1995; Milinski et al. 1995). As was found in these studdominant individuals, such as adult males, are almost ies, our distribution of phenotypes was not truncated
unaffected. A similar pattern of time maximization has between patches, contrary to the predictions of the
been described, at the interspecific level, in other scav- model. Our data show, however, that adult males search
enging guilds (Hiraldo et al. 1991). Such a strategy by on the plain more frequently than juvenile females
extremely subordinate condors would be facilitated by search in the mountains; this would fit a partial truntheir higher flying capabilities, which would permit them cationss (Milinski et al. 1995). This could be due to many
to remain for longer periods of time at carcasses.
factors, such as imperfect habitat knowledge, unstable
We detected a positive effect of the number of con- resource distribution and intraspecific kleptoparasitism
dors present on the individual rate of food intake. As (Sutherland and Parker 1986). In addition, other factors
occurs at the interspecific level in other scavenger as- such as the presence of dominants (see Houston 1988),
semblages (Alvarez et al. 1976), the presence of a larger the amount of carrion available, and the hunger level of
number of conspecifics probably determines some feed- the individual could influence the probability of landing
ing advantages that compensate for the inhibition ef- at a carcass. In fact it is well known that food-stressed
fects. A larger number of condors can better dismember individuals cover larger foraging distances and visit
the cadaver, permitting access to a larger amount of suboptimal areas (Village 1982; Bloom et al. 1993, Tella
food. Additionally, larger group sizes can reduce the et al., in press). Thus, dominant condors which have not
amount of time dedicated to vigilance, as has been ob- detected carcasses could visit plain areas, but the reverse
served in other social foraging species (Gluck 1986; Li- (extreme subordinates visiting carcasses) in the mounma and Dill 1990; Alonso and Alonso 1991). An tains would be less frequent, as we observed. It is worth
interesting observation, however, is that this effect was emphasizing that our three fitted GLM models acnot detectable for juvenile females. They spent almost counted heavily for the carcassss factor. This supports
the same amount of time feeding regardless of the the hypothesis that the conditions occurring at carcasses
number of conspecifics present. Juvenile females are can be highly variable.
probably not able to benefit from an increase in group
There may be an alternative explanation to habitat
size since all the birds present (when competitors are not segregation by despotic competition. Focusing their
present they would be other juvenile females) can po- searching and scavenging activities in plains, suborditentially compete with them for food.
nate condors could avoid eventual resource depletion
The second assumption was that the relative pay-offs in the mountains. This benefit could not be realized by
of phenotypes change between patches. We have ob- breeding adults, as their range movements would be
tained indirect evidence supporting this; the number of limited by nest site attendance. Thus, subordinate birds
64
would compensate for lower pay-offs in mountain
areas by exploiting a larger and consequently more
profitable area. A similar strategy of young nonbreeding subordinate birds versus breeding adults has
been described for other group-foraging species (Heinrich 1988, Donazar et al. 1996; Tella et al., in press).
In our opinion, however, our data better fit a scenario
of habitat segregation by despotic competence, since
non-breeding juvenile males did not show a similar
pattern as juvenile females, which would be expected if
segregation by constraints linked to breeding area fidelity are operating.
Foraging strategies and sex roles
Habitat segregation by despotic competence would increase the cost/benefit relationship for subordinate birds
since they should travel to more distant areas with a
higher mortality risk. A question arises from this scenario: how can these asymmetries be maintained within
an evolutionary context? In our opinion, the advantages
obtained by foraging extreme dominant birds (adult
males) would be compensated by higher costs in other
life history traits. Our results show that the fraction of
adult females among the scavenging birds in mountain
areas close to condor sites is much lower in the spring,
when nestlings are still growing, than in the summer,
when fledglings are almost grown up (see Palermo 1983
for condor breeding seasons). This suggests that parental sex roles in reproduction can be very different and
that the burden of nest and chick care must fall on the
females, while the male could be responsible for feeding.
A few observations conducted on captive breeding pairs
seem to support this hypothesis (Klos 1973, 1984). In
addition, Andean condors are known to perform complex courtship behaviours not found in any other species
of New or Old World vultures (Gailey and Bolwig 1973),
which seems to indicate the existence of selective pressures linked to sexual selection (Hedrick and Temeles
1989; Andersson 1994). As a synthesis of this reasoning,
it can be hypothesized that asymmetric advantages in
foraging activities and sexual selection constraints could
favour divergence in body size between the sexes and
explain this unusual pattern of sexual dimorphism
among raptors.
Acknowledgements. Obdulio Monsalvo, Javier Bustamante, Miguel Pineda and Martin Funes helped with the fieldwork. Our
thanks to Gerardo Alena, Gabriel and Miguel Anz, Raul Cordero,
Victor Soleno, and the administrators of the Estancias Cerro de los
Pinos, Chimehuin, Collon-Cura, Lolen, and Quemquemtreu, who
permitted us to work on their land. Ricardo R. Estrella, Jose L.
Tella and Manuela G. Forero improved earlier versions of the
manuscript. Logistic support was provided by the Centro de Ecologia Aplicada del Neuquen (Argentina); we are very grateful to
Alejandro del Valle and Antonio Guinazu for their continuous
help. Financial support was provided by the Instituto de Cooperacion Iberoamericana and the Ministerio de Asuntos Exteriores
(Spain) through the Programa de Cooperacion Cientifica con Iberoamerica. The second author (A.T.) had a postdoctoral fellowship
from the Ministerio de Educacion y Ciencia (Spain). Ignacia de
Bustamante, Dougie and Norina Lawson, and Andy Green translated the text into English.
References
Alonso JC, Alonso J (1991) Costs and benefits of flocking in
common cranes. In: Harris J (ed) Proceedings of the 1987 International Crane Workshop. International Crane Foundation,
Baraboo, pp 271—276
Alonso JC, Bautista LM, Alonso JA (1997) Dominance and the
dynamics of phenotype-limited distribution in common cranes.
Behav Ecol Sociobiol 40:401—408
Alvarez F, Arias de Reyna L, Hiraldo F (1976) Interactions among
avian scavengers in southern Spain. Ornis Scand 7:215—226
Anderson J, Horwitz RJ (1979) Competitive interactions among
vultures and their avian competitors. Ibis 121:505—509
Andersson M (1994) Sexual selection. Princeton University Press,
Princeton, NJ
Baker MC, Belcher CS, Deutsch LC, Sherman GL, Thompson DB
(1981) Foraging success in junco flocks and the effects of social
hierarchy. Anim Behav 29:137—142
Balph MH (1977) Winter social behaviour of dark-eyed juncos:
communication, social organization, and ecological implications. Anim Behav 25:859—884
Bautista LM, Alonso JC, Alonso JA (1995) A field test of ideal free
distribution in flock-feeding common cranes. J Anim Ecol
64:747—757
Bekoff M, Scott AC (1989) Aggression, dominance, and social
organization in evening grosbeaks. Ethology 83:177—194
Benkman CW (1988) Flock size, food dispersion, and the feeding
behavior of crossbills. Behav Ecol Sociobiol 23:167—175
Bloom PH, McCrary MD, Gibson MJ (1993) Red-shouldered
hawk home range and habitat use in southern California.
J Wildl Manage 57:258—265
Buckley NJ (1996) Food finding and the influence of information,
local enhancement, and communal roosting on foraging success
of North American vultures. Auk 113:473—488
Bustamante J, Donazar JA, Hiraldo F, Ceballos O, Travaini A
(1997) Differential habitat selection by immature and adult grey
eagle-buzzards Geranoaetus melanoleucus. Ibis 139:322—330
Cabrera AL (1976) Regiones fitogeograficas argentinas. Enciclopedia Argentina de Agricultura y Jardineria, tomo II,
fasciculo 1. Editorial ACME SACI, Buenos Aires
Caraco T (1981) Risk-sensitivity in foraging groups. Ecology
62:527—531
Clark C, Mangel M (1986) The evolutionary advantages of group
foraging. Theor Popul Biol 30:45—75
Crawley MJ (1993) GLIM for ecologists. Blackwell, London
Del Hoyo J, Elliot A, Sargatal J (1994) Handbook of the birds of
the world, vol 2. Lynx, Barcelona
Dobson AJ (1983) Introduction to statistical modelling. Chapman
& Hall, London
Donazar JA, Ceballos O (1988) Red fox predation on fledgling
egyptian vultures. J Raptor Res 22:88
Donazar JA, Hiraldo F, Bustamante J (1993) Factors influencing
nest site selection, breeding density and breeding success in the
bearded vulture (Gypaetus barbatus. J Appl Ecol 30:504—514
Donazar JA, Ceballos O, Tella JL (1996) Communal roosts of
Egyptian vultures (Neophron percnopterus): dynamics and implications for the species conservation. In: Muntaner J, Mayol J
(eds) Biologia y conservacion de las rapaces mediterraneas.
Sociedad Espanola de Ornitologia, Madrid, pp 189—201
Elosegi I (1989) Vautour fauve (Gyps fulvus), gypaete barbu
(Gypaetus barbatus), percnoptere dsEgypte (Neophron per
cnopterus): synthese bibliographique et recherches. Acta Biol
Mont 3:1—278
Fretwell SD (1972) Populations in a seasonal environment.
Princeton University Press, Princeton, NJ
65
Fretwell SD, Lucas HL Jr (1970) On territorial behavior and other
factors influencing habitat distribution in birds. Acta Biotheor
19:16—36
Gailey J, Bolwig N (1973) Observations on the behavior of the
Andean condor (Vultur gryphus). Condor 75:60—68
Garcelon DK (1990) Observations of aggressive interactions by
bald eagles of known age and sex. Condor 92:532—534
Gluck E (1986) Flock size and habitat-dependent food and energy
intake of foraging goldfinches. Oecologia 71:268—272
Goss-Custard JD, Clarke RT, Durell SEA (1984) Rates of food
intake and aggression of oystercatchers Haematopus ostralegus
on the most and the least preferred mussel Mytilus edulis beds
of the Exe estuary. J Anim Ecol 53:233—245
Hedrick AV, Temeles EJ (1989) The evolution of sexual dimorphism in animals: hypotheses and tests. Trends Ecol Evol
4:136—138
Heinrich B (1988) Winter foraging at carcasses by three sympatric
corvids, with emphasis on recruitment by the raven, Corvus
corax. Behav Ecol Sociobiol 23:141—156
Heinrich B (1994) Dominance and weight changes in the common
raven, Corvus corax. Anim Behav 48:1463—1465
Hiraldo F, Blanco JC, Bustamante J (1991) Unspecialized exploitation of small carcasses by birds. Bird Study 38:200—207
Houston DC (1988) Competition for food between Neotropical
vultures in forest. Ibis 130:402—417
Huntingford F, Turner A (1987) Animal conflict. Chapman & Hall,
London
Kirk DA, Gosler AG (1994) Body condition varies with migration
and competition in migrant and resident South American vultures. Auk 111:933—944
Kirk DA, Houston DC (1995) Social dominance in migrant and
resident turkey vultures at carcasses: evidence for a despotic
distribution? Behav Ecol Sociobiol 36:323—332
Klos H-G (1973) Hand-rearing Andean condors at West Berlin
Zoo. Int Zoo Yearb 13:112
Klos H-G (1984) Breeding history of the Andean condor at the
West Berlin Zoo. Int Zoo Yearb 23:14—16
Knight RL, Knight SK (1988) Agonistic asymmetries and the
foraging ecology of bald eagles. Ecology 69:1188—1194
Koford CB (1953) The California condor. Dover, New York
Krebs JR (1974) Colonial nesting and social feeding as strategies
for exploiting food resources in the great blue heron (Ardea
herodias). Behaviour 51:99—134
Lima SL, Dill LM (1990) Behavioral decisions made under the risk
of predation: a review and prospectus. Can J Zool 68:619—640
Lindstrom K, Ranta E (1993) Foraging group structure among
individuals differing in competitive ability. Ann Zool Fenn
30:225—232
McCullagh P, Nelder JA (1983) Generalised linear modelling.
Chapman & Hall, London
McGahan J (1972) Behavior and ecology of the Andean condor.
PhD thesis, University of Wisconsin.
McGahan J (1973) Gliding flight of the Andean condor in nature.
J Exp Biol 58:225—237
Milinski M (1988) Games fish play: making decisions as a social
forager. Trends Ecol Evol 3:325—330
Milinski M, Parker GA (1991) Competition for resources. In:
Krebs JR, Davies NB (eds) Behavioural ecology. Blackwell,
Oxford, pp 137—168
Milinski M, Boltshauser P, Buchi L, Buchwalder T, Frischknecht
M, Haderman T, Kunzler R, Roden C, Ruetschi A, Strahm D,
Tognola M (1995) Competition for food in swans: an experimental test of the truncated phenotype distribution. J Anim
Ecol 64:758—766
Monaghan P (1980) Dominance and dispersal between feeding
sites in the herring gull (Larus argentatus). Anim Behav
28:521—527
Monaghan P, Metcalfe NB, Hansell MH (1986) The influence of
food availability and competition on the use of a feeding site by
herring gulls. Bird Study 33:87—90
Mundy PJ (1982) The comparative biology of Southern African
vultures. Vulture Study Group, Johannesburg
Mundy PJ, Butchart D, Ledger J, Piper S (1992) The vultures of
Africa. Academic Press, London
Nelder JA, Wedderburn RWM (1972) Generalized linear models. J
R Stat Soc A 135:370—384
Palermo MA (1983) El condor. Fauna argentina 23. Centro Editor
de America Latina, Buenos Aires
Parker GA, Sutherland WJ (1986) Ideal free distributions when
individuals differ in competitive ability: phenotype-limited ideal
free models. Anim Behav 34:1222—1242
Pennycuick CJ (1972) Soaring behaviour and performance of some
East African birds observed from a motor-glider. Ibis 114:178—
218
Pulliam HR, Caraco T (1984) Living in groups: is there an optimal group size? In: Krebs JR, Davies NB (eds) Behavioural
ecology: an evolutionary approach. Blackwell, Oxford, pp 125—
148
Ranta E, Rita H, Lindstrom K (1993) Competition versus co-operation: success of individuals foraging alone and in groups.
Am Nat 140:42—58
Rita H, Ranta E, Peuhkuri N (1996) Competition in foraging
groups. Oikos 76:583—586
Schaller GB (1972) The Serengeti lion. University of Chicago Press,
Chicago
Senar JC (1994) Vivir y convivir, la vida en grupos sociales. In:
Carranza J (ed) Etologia, Introduccion a la ciencia del comportamiento. Universidad de Extremadura, Caceres, pp 205—
233
Senar JC, Camerino M, Metcalfe NB (1989) Agonistic interactions
in siskin flocks: why dominants sometimes subordinate?. Behav
Ecol Sociobiol 25:141—145
Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for the
behavioral sciences. New York, McGraw-Hill
Sutherland WJ, Parker GA (1985) Distribution of unequal competitors. In: Sibly RM, Smith RH (eds) Behavioural ecology.
Blackwell, Oxford, pp 255—274
Tella JL, Forero MG, Hiraldo F, Donazar JA (in press) Conflicts
between lesser kestrel conservation and European agricultural
policies as identified by habitat use analysis. Conserv Biol
Vickery WL, Giraldeau L-A, Templeton JJ, Kramer DL, Chapman
CA (1991) Producers, scroungers, and group foraging. Am Nat
137:847—863
Village A (1982) The home range and density of kestrels in relation
to vole abundance. J Anim Ecol 51:69—80
Wallace MP, Temple SA (1987) Competitive interactions within
and between species in a guild of avian scavengers. Auk
104:290—295
Ward P, Zahavi A (1973) The importance of certain assemblages as
information centresss for food-finding. Ibis 115:517—534
Wells H, King JL (1980) A general exact testss for N x M contingency tables. Bull S Calif Acad Sci 79:65—77
Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, Cambridge, Mass
Communicated by J. Hoglund