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The MosT exTreMe sexual size DiMorphisM aMong BirDs:
alloMeTry, selecTion, anD early Juvenile DevelopMenT
in The greaT BusTarD (Otis tarda)
R.
—Otis t arda es el ave con mayor dimorfismo sexual y una de las de mayor peso entre las que conservan la capacidad
de vuelo. Los machos adultos capturados en España fueron . veces más pesados que las hembras y sus medidas lineales un
–% mayores que las de las hembras. Entre finales del invierno y la estación reproductiva el peso medio aumentó en un % en
las hembras y en un % en los machos. El dimorfismo sexual se manifiesta en los pollos de esta especie a edades muy tempra nas, lo
que implica que los machos han de sufrir un mayor costo durante el crecimiento que las hembras. El peso y el dedo medio mostraron
en los machos un desarrollo hiperalométrico en relación con la longitud alar, mientras que estas medidas fueron isométricas en las
hembras. Además, dichas medidas fueron las que presentaron mayor variabilidad fenotípica de entre todos los caracteres biométricos
medidos en los machos, siendo éstas también más variables en los machos que en las hembras. Aunque la hiperalometría y una
mayor varianza han sido frecuentemente utilizadas como argumento para apoyar la selección sexual como fuerza evolutiva, nuestros
resultados sugieren que el peso y el dedo medio han sufrido procesos evolutivos diferentes. La competencia sexual entre machos es
muy marcada en esta especie, y un mayor peso facilita el acceso a las hembras. Por ello, la selección sexual ha debido favorecer un
incremento del peso hasta el límite impuesto por el beneficio derivado de seguir conservando la capacidad de vuelo. Por otro lado,
como Otis tarda es un ave p oco pro pensa a volar y que s e despl aza fun damenta lmente c ami nando, la h ipera lome tría del de do me dio
ha debido desarrollarse por selección natural, como respuesta al enorme peso, para cumplir adecuadamente la función de soporte y
mantenimiento del equilibrio.
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e Auk 126(3):657−665, 2009
e American Ornithologists’ Union, 2009.
Printed in USA.
e Auk, Vol. , Number , pages −. ISSN -, electronic ISSN - . by e American Or nithologis ts’ Union. Al l rights res erved. Please direct
all requests for permission to photocopy or reproduce article content throug h t he Universit y of Califor nia Press’s Rights and Permissions website, http://ww w.ucpressjourna ls.
com/reprintInfo.asp. DO I: . /au k. .
El Mayor Dimorfismo Sexual en Tamaño entre las Aves: Alometría, Selección y Desarrollo Temprano
del Dimorfismo en los Jóvenes de Otis tarda
Ju a n C. al o n s o ,1,3 Ma r i n a Ma g a ñ a ,1 Ja v i e r a. al o n s o ,2 Ca r l o s Pa l a C í n ,1
Ca r l o s a. Ma r t í n ,1,4 a n d Be a t r i z Ma r t í n 1
1Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales , Consejo Superior de Investigaciones Científicas, José Gutiér rez
Abascal 2, E-28006 Madrid, Spain; and
2Departamento de Biología Animal, Facultad de Biología, Universidad Complutense, E-2804 0 Madrid, Spain
3E-mail: jcalonso@mncn.csic.es
4Present address: Instituto de Investigación en Recursos Cinegéticos, Consejo Superior de Investigaciones Científicas—Universidad de Castilla-La
Mancha, Ronda de Toledo s/n, E-13071 Ciudad Real, Spain.
A.—e Great Bustard (Otis tarda) is one of the heaviest flying birds and the most sexually dimorphic living bird. Adult
males weighed .× more than females, and their linear measurements were –% larger. Weight increased between the pre-
breeding and breeding seasons by % in females and % in males. Sexual size dimorphism emerges very early in development and
explains why growth in males is so costly. Weight and central toe length were hyperallometric when related to wing length in males but
isometric in females and varied more in males, as compared with females and with other male traits. Although hyperallometry and high
variability have frequently been used to invoke sexual selection as a driving force, our results support different functional hypotheses for
the evolution of each trait. Male–male competition is intense in this lekking species, and high rank among males and access to females
are weight-dependent. us, sexual selection has likely pushed male weight close to the limit imposed by powered flight. Because Great
Bustards are mostly cursorial, the hyperallometry of the central toes of males in relation to wing length most likely evolved for support
and balance. Received November , accepted March .
Key words: allometry, body size, Great Bustard, Otis tarda, sexual selection, sexual size dimorphism.
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A
dimorphism (SSD) may have evolved
by natural selection through niche divergence processes, agonistic
and epigamic sexual selection are probably the main mechanisms
leading to sex differences in size. e common view at present is
that sexual segregation in different niches may help maintain SSD,
rather than being the driving force underlying it (Ruckstuhl and
Neuhaus , Fairbairn et al. ).
e best way to estimate the influence of sexual selection
on a male trait is by measuring lifetime multivariate selection
on the trait in natural populations. Because this is generally dif-
ficult, experimental manipu lation of the trait or study of static
allometr y is often used to infer selection. Using verbal models,
several authors have suggested that allometric coefficients in
excess of those expected by isometr y (hyperallometry) would
evolve in traits subject to sexual selection, whereas isometry or
hypoallometry would be expected for traits under natural se-
lection (Green , Petrie ). However, recent studies have
contradicted these assumptions, and the issue remains contro-
versial (Bonduriansky and Day , Eberhard , Bertin and
Fairbairn ).
Here, we present data on SSD and scaling among body
weight and various linear morphometric tra its in the Great
Bustard (Otis tarda). is species is a good candidate for inves-
tigating the selective pressures that potentially lead to sexual
differences in size, for at least four reasons. First, it is one of the
largest flying birds: the male’s maximum weight of ~ kg is sim-
ilar to that of other large bustards, such as the Kori Bustard (Ar-
deotis kori; del Hoyo et al. ). Second, Great Bustards are one
of the most sexua lly dimorphic birds. In a review of SSD in birds,
Pay ne () listed the Gre at Bustard a s t he second most di mor-
phic in wing length in the family Otididae. ird, Great Bustards
mate in leks, and less than half the males on a lek may copulate;
weight and age strongly contribute to rank in the male hierarchy
and to mating success (Magaña ). Males show their status
and body condition through their secondary sexual traits (whis-
kers and neck development and color) and fight by gripping each
other with their bills and shoving and jostling breast-to-breast,
sometimes for > h. In captivity, weight increases in spring have
been reported for three large bustards, though samples were
small: Australian Bustard (A. australis; Fitzherbert ), Great
Bustard (Carranza and Hida lgo ), and Kori Bustard (S. Hal-
lager pers. comm.). If a spring weight increase occurs in the wild,
it could confer vital physiological and fighting advantages during
the long period the birds spend on leks. Fourth, male and female
Great Bustards live in separate flocks all year round, which raises
the possibility that their extreme sexual dimorphism evolved
through niche specialization.
is paper accomplishes three objectives. First, we present
body measurements of a large sample of free-living Great Bustards
of both sexes. is is the first detailed account of SSD and of sea-
sonal weight changes for any of the extremely large and dimorphic
bustards. Second, we discuss the allometric constants, presenting
various body measurements in relation to what might be expected
from sexual and natural selection. ird, we explore the extent to
which the allometric relationships and SSD of adults are present
in juveniles and compare our results with published data on other,
less dimorphic birds to infer whether the growth rate of males is
limited by energy requirements.
Me t h o d s
Data collection and variables analyzed.—We analyzed the biom-
etry of a sample of Great Bustards ( adult males, adult
females, juvenile males, and juvenile females) captured in
Spain between and . Adults were captured at several leks
or foraging areas between early January and early April, –
, mostly in central Spain using rocket nets. Great Bustards
live in flocks at this time of year, so captures were not selective
with respect to age, size, or social status and should be a random
sample of the population. Because birds were captured for behav-
ioral ecology studies, we released them within a few minutes to
minimize capture stress; thus, for many birds we measured only
weight and wing arch. Immature males (i.e., those in their third
calendar year or younger; Gewalt , Alonso et al. ) were
excluded from the sample. Females reach sexual maturity at age
two (much earlier than males), and year-old and older females can-
not be distinguished, so our sample of females may include some
year-old birds. Dependent young were captured between and
in Madrid, Zamora, Navarra, and several Andalusian prov-
inces in the second half of July, when they were – days old,
and released within min after capture. In all cases, they were
soon rejoined by their mothers. We sexed all birds through dis-
criminant analysis of their body measurements and some also
with molecular techniques. e ages of young birds were esti-
mated with second-order polynomic growth curves for body mass
using a sample of males and females reared in –
at the breeding station in Buckow, Germany (H. Litzbarski and T.
Langgemach pers. comm.). To check for possible errors when cal-
culating SSD values of young birds because of potential sex-bias in
capture success, we used the subsample of sibling pairs wherein
one chick was female and the other was male. Our morphological
measurements are defined in Table . Weight was measured to the
nearest g using -kg or -kg Pesola scales. Wing arch, wing
chord, and tail lengths were measured to the nearest mm, and
all other measurements were measured to the nearest . mm. All
measurements were made by J.C.A.
Statistical analyses.—To test for possible seasonal variation, we
divided our adult sample into two groups: pre-breeding birds (cap-
tured before March) and breeding birds (captured after that date).
Great Bustards are globally endangered and are strictly protected in
Spain, so our breeding sample is small, because most trapping oc-
curred in winter to avoid interfering with breeding. We analyzed
seasonal and sex differences using t wo-sample Student’s t-tests on
log-transformed variables. For sibling pairs, we used Wilcoxon’s
matched-pairs test. We used principal component analyses (PCA)
and Pearson r correlation matrices for both adults and juveniles to
explore the general biometric patterns within sexes and differences
between the sexes. We used STATISTICA, version . (StatSoft,
Tuls a, Ok laho ma), fo r these an alys es, a nd al l tes ts were t wo-t ailed .
To analyze sex differences in allometric scaling, we regressed
log (Yi) on log (wing arch), where Yi represents our various morpho-
logical measurements; males and females were analyzed separately.
We used wing arch as our measure of body size because it loaded
heavily on the first principal component (PC) and because we had
many wing-arch measurements. We used reduced major-axis re-
gression (RMA) because it is preferred over least-squares regres-
sions in scaling studies where X and Y variables have different units
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such as length and mass (Harvey and Pagel ). Observed slopes
were compared with those predicted from allometry to identify
characters that had hyperallometric scaling. For linear measure-
ments regressed on wing arch, the expected allometric constant
should be ., and for mass it should be . (Schmidt-Nielsen ).
Re s u l t s
Weight and other measurements of adult birds.—Adult males were
much larger than adult females in all morphometric variables,
with no overlap between the ranges of both sexes for any measure
(Table ). ere were significant seasonal weight increases in both
sexes (Table ). ese increases were equivalent to % of the pre-
breeding weight in males, and % in females. ese seasonal dif-
ferences have to be considered when reporting mean weights for
this species and comparing them with values for other species. For
example, in our study, where the pre-breeding and breeding sam-
ple sizes differed markedly, a more representative mean weight for
male Great Bustards would be . kg, the average between the
pre-breeding (. kg) and breeding means (. kg). is aver-
age is notably higher than the overall mean given in Table . As
for the male whiskers, it is well known that they start growing in
Ta B l e 1. Weight (kg) and linear measurements (mm) of adult and juvenile Great Bustards taken in the present study.
Wing ar ch Maximum distance between carpal joint and tip of the longest primary, measured with a tape along the dorsal side of the wing
Wing chord Minimum distance between carpal joint and tip of the longest primary feather (unflattened wing length)
Tail length Length of the longest tail feather, pushing the bottom of the ruler gently against the base of the middle pair of rectrices while
the tail is folded naturally
Tarsus length Distance between the notch on the back of the intertarsal joint and lower edge of the last complete scale before the toes diverge
Central toe length Distance between distal end of tarsus and central toe tip excluding the claw, with the toe stretched
Head length Maximum distance between the occipital end of the head and the tip of the bill
Head width Maximum width of the skull behind the eyes
Bill length 1 Distance between the posterior end of bill commisure and bill tip
Bill length 2 Distance between the anterior end of nostrils and bill tip
Length of whiskers Length of the longest whitish barbs that arise from each side of the chin, measured from the bill tip on the right side (measured
only in adult males; these feathers develop much less and only occasionally in adult females)
Number of
whiskers
Number of true barbs, which can be distinguished from the rest of the chin feathers by their characteristic morphology (Gewalt 1959),
counted on the right side (in adult males)
Weight Measured in kilograms
Ta B l e 2. Weight (kg) and linear measurements (mm) of adult Great Bustards. All sexual differences were highly significant (P < 0.001). Coefficients of
variation (CV) and sexual-size-dimorphism values (SSD, expressed as male:female) are also given.
Males Females
Measure Mean SD Range CV nMean SD Range CV nSSD
Weight
a,b 9.82 1.18 7.0–13.0 12.0 6 155 4. 35 0.47 3.30–5.20 10.86 51 2. 26a
Length of whiskers 215.1 26.1 15 0 –2 70 12.12 97 — — — — — —
Number of whiskers 14.5 4.8 7–30 32.8 0 74 — — — — — —
Wing ar ch 628.0 19.2 570– 685 3.05 92 491.5 16. 3 435 –525 3.31 28 1.28
Wing chord 566.9 14.7 535 – 610 2. 59 50 444.7 14.7 400 – 470 3.30 19 1. 27
Tail length 265.0 12.0 24 0 –295 4.53 46 2 24.7 8.0 210–240 3.57 10 1.18
Tarsus length 152. 7 7. 3 138 –17 6 4.81 59 120.0 5.6 112. 5 –129.5 4.63 14 1.27
Central toe length 69.9 4.3 58.5–79.2 6.22 48 53.7 1. 6 49.5 –55.6 3.06 15 1. 30
Head length 151.1 4.8 134.5–160.5 3.20 54 12 2. 3 3.3 11 5. 5 –1 29 .7 2.71 18 1.24
Head width 54.7 1.8 51.3–58.5 3.37 44 46.0 1.6 44.6–48.4 3.40 51.19
Bill length 1 88.9 3.6 80.5–98.6 4.01 44 73.9 4.5 68.0–78.7 6.03 51. 20
Bill length 2 34.4 1.4 31–37 4 .18 45 2 7. 8 1.6 24.4– 29.8 5.68 10 1. 24
a Mean annual weights calculated by averaging means of the pre-breeding and breeding samples were identical to the overall means given in this table for females (4.35 kg)
but were notably higher in males (10.64 kg), resulting in an SSD value of 2.45 (SSD pre-breeding = 2.40, SSD breeding = 2.48; see text).
b
A 19-kg male found dead on 3 February 2009 in southeastern Spain was reported to us by S. Villaverde, Centro de Recuperación de Fauna de Albacete (not included in
the analyses of the present study).
Ta B l e 3. Seasonal changes in weight (kg) of adult Great Bustards (***P < 0.001) .
Pre-breeding Breeding Difference
Mean Range SD nMean Range SD n t-test
Males 9.65 7.00–12.00 1.03 141 11.6 2 9 .5 0 –13. 0 0 1.20 14 6.19** *
Females 4.02 3. 30 –4.45 0.35 26 4.68 3.85 –5.20 0.30 25 6.86***
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December, increase in number and length up to the peak mating
season in late April, and are lost during the prebasic molt (Gewalt
, Alonso et al. , Magaña ). Linear measurements of
size did not change with season.
Controlling for seasonal variation by considering separately
the pre-breeding and breeding samples and excluding whisker
length and number, weight was the measure that showed the high-
est interindividual variability in adults of both sexes, with higher
values for males than for females (coefficient of variation [CV] =
.% and .% in males and .% and .% in females in the
pre-breeding and breeding samples, respectively). Central toe and
tarsus length were the next most variable traits in males, more
variable than in females (Table ). In young birds of both sexes,
weight and tail length showed the highest variability, and head
length and head width the lowest (Table ).
Morphometric patterns: Sex and age differences.—In adults,
the correlation matrices of both sexes were very similar. e
main sexual differences among adults were in central toe, tarsus,
and tail lengths. In males, central toe length was highly corre-
lated with weight, tarsus, head, and both measures of bill length
(respectively, r = ., ., ., ., and .; n = males),
whereas in females central toe length was correlated with tail
le ngth (r = . , n = females) but clearly not with weight, tarsus,
and head lengths (respectively, ., −., .; n = females).
Tail length showed few correlations with other measurements in
males (only with wing chord: r = ., n = ) and in females (with
central toe and bill length : respectively, r = ., r = .; n = ).
Tarsus length was correlated only with central toe and bill length
in males (respectively, r = ., r = .; n = ) and with head
length in females (r = ., n = ). In young birds of both sexes,
the correlations between a ll bo dy mea surements were high ly sig-
nificant (P < .; P < . in the subsample of sibling pairs,
values not shown).
e results of principal component analyses confirmed these
relationships and showed similar morphometric patterns between
adults and juveniles (Table ). PC was defined by strongly negative
values for all linear measurements and weight in adults and in both
samples of juveniles, thus reflecting the overall size of the birds. is
factor explained most of the variance, in both adults and juveniles.
Sexual size dimorphism in adults and juveniles.—Both ju-
venile and adult males were much larger in all body measures
than females (Tables and ). Adult and juvenile males showed
significantly higher values of PC, the factor reflecting overall
body size (adults: F = ., df = and , P < .; all juve-
niles: F = ., df = and , P < .; subsample of juve-
nile sibling pairs: F = ., df = and , P < .). In adults,
SSD was greatest for weight, with males weighing .× more
than females (Table ). Weight dimorphism was even higher
when the pre-breeding and breeding samples were analyzed sep-
arately (males:females pre-breeding = ., males:females breed-
ing = .; Table ). High SSD values in adults also were found in
central toe, tarsus, and wing arch and chord, all of which were
–% longer in males. Tail length showed the lowest SSD val-
ues (Table ).
In young birds, all dimorphism coefficients were some-
what smaller, but general trends were similar to those for adults,
with highest values in weight and central toe and tarsus lengths
(Table ). All body parts grew quickly in juveniles, reaching, at
Ta B l e 4. Weight (g) and linear measurements (mm) of young Great Bustards. All sexual differences were highly significant (P < 0.001). Sexual-size-dimorphism values (SSD, expressed as
male:female) are also given.
Males Females SSD
21 sibling pairs All juveniles 21 sibling pairs All juveniles
Measure Mean SD CV Mean SD CV nMean SD CV Mean SD CV n21 sibling pairs All juveniles
Weight 2 ,160. 7 445.4 20.6 2,135.4 608.9 28.5 286 1,383.1 2 47.1 17.9 1,392. 2 332. 2 23.9 275 1. 56 1. 53
Wing ar ch 429.4 4 7. 5 11.1 430.7 50.2 11. 6 282 376 .8 35.6 9.4 381.9 37. 5 9.8 271 1.14 1.13
Wing chord 384 .1 42.6 11.1 3 8 7. 7 45 .1 11. 6 282 342.0 31.3 9.2 3 4 7. 8 34.4 9.9 270 1.12 1.11
Tail length 18 7. 5 2 7. 7 14.8 186 .5 32.1 17. 2 286 174.1 21.1 12.1 175. 4 22.8 13.0 274 1. 08 1.0 6
Tarsus length 120. 0 10. 2 8.5 121. 8 13. 8 11. 4 283 103.7 8.0 7.7 106 .9 10 .1 9.4 273 1.16 1.14
Central toe length 57. 9 4.3 7.4 58.7 5.2 8.9 281 48.0 3.1 6.5 49.5 3.6 7. 4 273 1. 21 1.19
Head length 111. 4 7.1 6.4 112 . 2 7. 6 6.8 284 98.2 4.5 4.6 99.8 5.8 5.8 271 1.13 1.12
Head width 41. 2 2.7 6.6 41. 4 2.7 6.5 282 3 7. 0 1. 7 4.6 3 7. 5 1.9 5.1 272 1.11 1.10
Bill length 1 64.4 4.6 7. 1 65.5 5.4 8.2 282 56.0 3.2 5.7 5 7. 6 4.0 7. 0 272 1.15 1.14
Bill length 2 22.6 2.1 9.3 22.8 2.3 10.0 284 20.1 1. 3 6.2 20.7 1. 7 8.0 271 1.12 1.10
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ta B l e 6. Weight (g) and linear measurements (mm) of young Great Bus-
tards at age 70 days, as predicted from second-order polynomic growth
curves adjusted to the sample of all juveniles. The values are the mea-
surements of juvenile birds expressed as percentages of adult values.
Males Females
Measured
at 70 days
Percentage
of a dult va lue
Measured
at 70 days
Percentage
of a dult value
Weight 3 ,157 32.1 2,003 46.0
Wing ar ch 5 01. 2 79.8 424.3 86.3
Wing chord 4 47. 2 78.9 388.9 8 7. 5
Tail length 226.8 85.6 207. 7 92.4
Tarsus length 140.9 92.3 121.1 10 0.0
Cen tral t oe length 65.3 93.3 53.0 98.7
Head length 123.8 81.9 10 7. 8 88.1
Head width 45.3 82.7 40 .1 8 7. 2
Bill length 1 73.8 83.0 63.5 86.0
Bill length 2 25.9 75.2 22.9 82.2
the age of days, .–% of the adult linear measurements
and .% (males) to .% (females) of the adult weight (Table ).
At that age, all measures were smaller in young females but rep-
resented higher percent values of the adult values than those of
young males. All measures had higher CV values in young males
(Table ). In both sexes, central toe and tarsus were the body parts
that reached the highest percent value of the adult measure (Ta-
ble ). ese were also the traits reaching highest SSD at the age
of days. e growth curves followed a similar pattern for all
body measures (see Fig. for an example). e growth rate was
only slightly higher for juvenile males between hatching and the
age of ~ days but later tended to diverge between sexes, when
female growth rate began to decline. e central toe represents an
extreme case of fast growth, with female and male chicks having
reached, at the age of days, .% and .% of the adult values,
respectively (Fig. ).
Scaling in adult birds.—When related to wing chord as an in-
dex of body size, weight and central toe length were hyperallo-
metric in males (Table ). In adult females, no measure deviated
significantly from isometry, but sample sizes for females were
small. More importantly, the slope of weight was . in females,
practically equal to that expected under isometry (.). For all
measures except bill length and , the allometric slope was more
positive in males than in females, though sex differences did not
reach statistical significance.
di s c u s s i o n
Maximum weights of adult males.—e maximum weight we re-
corded for male Great Bustards was kg, which is notably lower
than the highest values cited in the literature for Iberian and cen-
tral European Great Bustards, – kg (Trigo de Yarto )
and – kg (del Hoyo et al. ), respectively. However, a male
found dead in Albacete, southeastern Spain, on February
weighed kg (S. Villaverde, Centro de Recuperación de Fauna
de Albacete, pers. comm.). Gewalt () cast some doubt on the
veracity of several old references reporting maximum weights of
up to – kg and suggested that “weights over kg are prob-
ably found only occasionally and under very favorable conditions.”
Although mean or maximum weights may have decreased during
the past century as a result of food availability or global warm-
ing (e.g., Yom-Tov ), we think that most old references close
to or exceeding kg should be considered exaggerations from
hunters either in central Europe or in Iberia. On the other hand,
we should allow for a further small seasonal increase of the maxi-
mum weights recorded in our sample up to the peak of the mating
Ta B l e 5. Results of the principal component analyses (PCA) of morpho-
metric measurements in adults (45 males and 10 females), juvenile sib-
ling pairs (21 males and 21 females), and all juveniles (275 males and 266
females). Only values for the first principal component (PC1) are given;
all other factors had eigenvalues <1.
Adults
PC1
Juveniles
(sibling pairs)
PC1
All
juveniles
PC1
Weight − 0.915 −0.926 −0.640
Wing ar ch −0.948 −0.955 − 0.958
Wing chord −0.950 −0.944 −0.951
Tail length −0.789 −0.832 −0.854
Tarsus length − 0.894 − 0.962 −0.956
Central toe length −0.885 − 0.913 −0.9 06
Head length −0.944 −0.979 −0.973
Head width
a—−0.956 −0.939
Bill length 1
a—−0.962 −0.954
Bill length 2 −0.903 − 0.910 − 0.851
Eigenvalue 6.55 8 .74 8.16
Percent variance 81.8 8 8 7. 37 81. 58
a These variables were omit ted in the principal component analyses of adults
because of the small sample size of females (see Table 2).
Fig . 1. Growth of central toe with age in Great Bustards 30–80 days old
(sample of all juveniles: 281 males and 273 females). Squares on the right
are the mean weights of adult birds (males: open square, females: black
square).
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season in late April (see below). erefore, ~ kg may be the max-
imum weight of male Great Bustards in Iberia, although some ex-
ceptional individuals may reach higher weights.
Seasonal variation in adult weight.—Results in the present
study are the first to show a spring weight increase in male and
female adult Great Bustards in the wild (Table ). Carranza and
Hidalgo () recorded similar increases in two of eight captive
birds. is increase is partly attributable to the development of
the subcutaneous tissue and of two profusely irrigated lobes in the
neck, which may reach kg weight in spring (Gewalt ). We
have no weight data for other seasons, but the scarce data from
captive birds (Carranza and Hidalgo ), the undernourished
appearance of males after the mating period, and the higher mor-
tality observed during the post-reproductive period (Martín ,
J. C. Alonso et al. unpubl. data) suggest that males probably reach
minimum weights in summer, as a consequence of the physical
strain suffered during male competition and mating (Magaña
). We also found a significant weight increase in females be-
tween the pre-breeding and breeding seasons, which probably re-
flects an accumulation of reserves for breeding.
Increases in weight of males in spring have been reported for
other large bustards in captivity: up to % in Australian Bustard
(A. australis; Fitzherbert ) and % in a male Kori Bustard (S.
Hallager pers. comm.). In wild male Kori Bustards, no signifi-
cant increase was observed between the dry season (. kg, n = )
and the wet season, when birds breed (. kg, n = ; T. Osborne
pers. comm.). Male weight also increased in spring in both sub-
species of the Houbara Bustard (Chlamydotis u. undulata and
C. u. macqueenii; Jacquet ).
Are Great Bustards the heaviest flying birds?—Our highest
weights did not reach those reported for the somewhat taller Kori
Bustards, which could also be somewhat exaggerated: .–. kg
(del Hoyo et al. ) and kg (reached by a captive male; S. Hal-
lager pers. comm.), but the male Great Bustard cited above, re-
cently reported from Albacete, indeed reached kg. e only
sample of wild Kori Bustards taken in recent times yielded a mean
weight of . kg for adult males (range: .–.; n = adult
males in Namibia, –; T. Osborne pers. comm.). is
weight is higher than our overall mean (. kg, t = ., P = .),
but the mean for the wet season (. kg) was not significantly
higher than our breeding-season mean (. kg, t = . , P = .).
Wild female Kori Bustards were larger and heavier (mean weight =
. kg, range: .–. kg, n = adult females; T. Osborne
pers. comm.) than our female Great Bustards, considering either
the total or only the breeding-season samples (P = . in both
cases). Male Kori Bustards seem to be as heavy as male Great Bus-
tards, but Great Bustards are more sexually dimorphic in weight
(male:female = . in the breeding season) than Kori Bustards
(male:female = . in the whole sample, . in the wet season).
Li mi ted d ata for Gre at I nd ia n Bu st ard s ( A. nigriceps; males almost
twice as heavy as females [Rahmani and Manakadan ]; males
≤. kg, females .–. kg [Rahmani , del Hoyo et al. ])
and Australian Bustards (del Hoyo et al. ) also indicate lower
SSD values in these species.
Mute Swans (Cygnus olor) and Andean Condors (Vultur gry-
phus) are similar (males: .– kg and – kg, respectively; del
Hoyo et al. , ; recent sample of Mute Swan males: .–
. kg, n = , BTO ), but less dimorphic, than Great Bustards.
Other birds with high male:female weight ratios are the Australian
Brown Songlark (Cincloramphus cruralis), at . (Amadon );
Capercaillie (Tetrao urogallus), at .–. (Milonoff and Lindén
); and Musc ov y D uck (Cairina moschata), a t ~. (F ai rba ir n et
al. ). Male:female ratios for linear measurements in Kori Bus-
tards varied between maximum values of . and . for tarsus
width and head length, respectively, and minimum values of .
and . for tarsus length and tail length, respectively (T. Osborne
pers. comm.). Great Bustards were more dimorphic in all mea-
sures except head length. In Great Indian Bustards, SSD for linear
mea sure ments va ried between . and . (Rah mani ).
In sum, Great Bustards show the highest sexual dimorphism,
in weight and in most linear measurements, known in birds.
Among terrestrial vertebrates, the SSD of Great Bustards is sur-
passed only by the most dimorphic mammals and some reptiles
(reviewed in Weckerly , Fairbairn et al. ). Male Great and
Kori bustards have comparable mean and maximum weights and
may be considered the two heaviest flying birds, on the basis of re-
cent samples taken in the wild.
Causes of SSD in adults.—Weight and central toe length were
hyperallometric in males but isometric in females and were more
variable in males as compared with females and with other male
traits. Nevertheless, our results did not support an association be-
tween allometry and sexual selection. Although hyperallometry
ta B l e 7. Scaling of morphometric measures against body size (wing chord), by sex, of adult Great Bustards. The reduced major-axis regression (RMA)
slope expected under isometry is 3 for weight and 1 for all other variables (*P < 0.05).
Males Females Sex difference
Test isometry:
males
Test isometry:
females
Variable RMA slope r n RMA slope r n T
adf T
adf T
adf
Weight 5.805 0.367 49 3.054 0.617 19 1.244 33 2 .113* 46 0.0 41 16
Tail length 1.732 0. 324 47 —b— — — — 1.692 45 — —
Tarsus length 1.54 4 0.120 61 1.49 8 0.150 14 0.045 18 1.4 6 0 61 0.615 14
Central toe length 2.020 0 .149 49 1. 373 0.117 11 0.506 15 2.117* 48 0 .416 11
Head length 1.042 0.262 49 0.793 0 .561 15 0.466 20 0.127 47 0.438 13
Head width 1.319 0 .14 0 46 —b— — — — 0.806 46 — —
Bill length 1 1. 312 0.209 45 —b— — — — 0.791 44 — —
Bill length 2 1. 351 0.209 46 —b— — — — 0.886 45 — —
a
The T statistic has the same distribution as Student’s t.
b The values for variables with n ≤ 10 were not significant; they are not given because of low sample size.
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and high variability are often interpreted as consequences of sex-
ual selection (e.g., Green , Petrie , Pomiankowski and
Moller , Eberhard et al. , González-Solís ), recent
empirical studies and analytical models have shown that some
sexually selected male traits may exhibit isometric or hypoallo-
metric scaling; thus, the form of selection operating on traits can-
not be reliably inferred from allometry patterns or trait variation
(Bonduriansky and Day , Bertin and Fairbairn ). Bon-
duriansky and Day () concluded that sexual selection would
result in positive allometry when the marginal fitness gains from
an increase in relative trait size are greater for larger individuals
than for smaller ones. is may be the case with regard to weight
in male Great Bustards, in which, as described below, the higher
mating success of heavier and older individuals suggests that sex-
ual selection may have favored heavier weights but not longer cen-
tral toes.
e allometric coefficient of . for male weight on wing arch
greatly exceeds the expected value of .. In Great Bustards, wing
length increases in males until they are – years old (i.e., well
beyond sexual maturity; Magaña ). Older males might ben-
efit more than younger males from becoming heavier because in-
creased weight (stored reserves, greater muscle mass, or larger
necks) and old age independently contribute to increasing their
mating success (Magaña ). In several mammals, efficiency
of antlers or tusks used in male–male fights increases with body
size and weight (reviewed in Andersson ). Because male Great
Bustards do not have weapons, body weight may be crucial in
male–male contests. ese combats may be dangerous, given that
males often peck their rival ’s face and eyes (J. C. Alonso et al. pers.
obs., using decoys). After such intense fighting, males are some-
times so exhausted that they temporarily cannot fly. Finally, being
heavy is not an obstacle in a species that displays on the ground.
On the contrary, it probably means more reserves that may be use-
ful during the peak mating season in April, when males spend only
% of their time feeding. Males that weighed more at the start of
the season spent less time feeding (r = −., n = , P = .; J. C.
Alonso et al. unpubl. data), which allowed them to concentrate on
display (Magaña ).
e central toe was also hyperallometric in males in relation
to wing chord, and central toe and tarsus were the two traits that
were the most sexually dimorphic, as well as the most variable
among males. e greater SSD of these skeletal structures may be
a consequence of being much heavier. Rather than being a result
of sexual selection, the development of longer toes and tarsi was
probably necessary to allow heavy males to keep their balance,
which is important in a species that is mostly cursorial. Central
toe length was positively correlated with weight, tarsus, head, and
bill lengths in adult males, but not in females. Also, the allometry
of central toe length on weight was ., not significantly different
from the value of . expected if the toe length is adjusted to the
mass the toes support. We interpret these relationships as sexual
selection having favored the extreme SSD in Great Bustards, lead-
ing to heavy weights only in males, which have developed strong
tarsi and long central toes as adaptations to support their huge
weights.
Other authors have found hyperallometric relationships
in body parts that are not explained by sexual selection but that
are also associated with larger or heavier individuals. Examples
are the tails of newts, which allow a greater propulsive force dur-
ing swimming (Green ); the width of atlas vertebrae of the
Caribou (Rangifer tarandus), which are hyperallometric because
of the relatively greater mass of muscles that has to be supported
in larger individuals (Hardy and Stroud ); the relatively lon-
ger wing-bones in larger birds, which are probably related to lift
requirements and size-dependent variation in flight behavior
(flapping vs. soaring; Nudds ); and the longer legs of larger
individual aquatic insects and spiders, which enable locomotion
on the water surface (Klingenberg and Zimmermann , Suter
and Gruenwald ). Likewise, wing dimorphism of some birds
has been interpreted as a need to provide aerodynamic compen-
sation for their sexually selected long tails (Andersson and An-
dersson ). ese size-required allometric increases describe
changes in form required to maintain a given function and, thus,
may be interpreted as functional constraints on shape imposed by
changes in size (“allometric constraint”; Fairbairn ).
e alternative hypothesis that SSD in weight and central toe
length were selected through sexual segregation seems unlikely.
Male and female Great Bustards occur in different flocks year
round but use the same areas and habitat types and have similar
foraging and locomotion strategies, and apparently they have no
significant dietary specializations (J. C. Alonso et al. pers. obs.).
Sexual segregation is common in several other game birds, as well
as in size-dimorphic ungulates, in which asynchrony in activity
budgets caused by sexually selected size dimorphism has been
suggested to make group cohesion costly to maintain (Ruckstuhl
and Neuhaus ). Natural selection may even work against sex-
ual selection for larger male size (a process for which evidence is
still sparse; see Blanckenhorn ) through mechanisms such as
() predation pressure against large, less agile males with reduced
ability to escape by flying or reduced maneuverability during flight
and () male vulnerability during food shortages. Finally, we do
not think that larger central toes are related to display-agility in a
species with ground display (Raihani et al. , Fairbairn et al.
), apart from the purely mechanical function of support-
ing the male’s weight. A recent review revealed SSD in birds to
be explained most consistently by sexual selection through mat-
ing competition, and the relationship of SSD in bustards was the
opposite of that predicted by the resource-division hypothesis
(Fairbairn et al. ).
Early development of SSD in the Great Bustard.—Great Bus-
tards show one of the most extreme cases of early SSD develop-
ment among sexually dimorphic birds (Teather and Weatherhead
, Fairbairn et al. ). Our results from a previous study
suggested how sexual selection may have favored rapid growth of
young males by increasing their competitive ability during the im-
mature period and probably also their fitness as breeding adults
(Alonso et al. ). Young males that fed at higher rates or re-
ceived more feedings from their mothers became independent at
a younger age, integrated earlier into adult male flocks, and set-
tled earlier at their definitive leks. However, these benefits of rapid
growth were counterbalanced by increased mortality (Martín et
al. ). As in several birds and mammal species, male-biased ju-
venile mortality resulting from starvation when food is scarce may
limit the growth rate of male Great Bustards (e.g., Clutton-Brock
, Torres and Drummond ). e resulting tradeoff means
that males grew more slowly than females when growth rates were
19_Alonso_08-233.indd 663 7/21/09 9:29:50 AM
664
—
al o n s o e t a l .
—
au k , vo l .
126
examined in relation to adult size, as has been shown for other di-
morphic birds (Teather and Weatherhead ). e male:female
weight ratio at fledging in Great Bustards and in another highly
dimorphic bird, the Capercaillie (. at an age of days in both;
fig. in Milonoff and Lindén , present study), is lower than
those of other birds with lower adult SSD values (fig. in Teather
and Weatherhead ) and confirms the main prediction of the
energetic-cost hypothesis (i.e., that a reduced male growth rate
should be most pronounced in the most dimorphic species). In-
stead of growing at the fastest possible rate, as predicted by the
allometry hypothesis of Teather and Weatherhead (), young
male Great Bustards continue putting on weight for a longer time
(up to – years; Magaña ), a pattern that is widespread
among dimorphic mammals (see Teather and Weatherhead ).
Indeed, for some male characters, asymptotic growth is achieved
after sexual maturity (Magaña , J. C. Alonso et al. unpubl.
data), a pattern found in many invertebrates, poikilothermic ver-
tebrates, and some highly dimorphic mammals, but rarely in birds
(Stamps ).
As in adults, the character that exhibited the most SSD in
juveniles was the length of the central toe, followed by tarsus
length. In males, the central toe grows through the immature
period and even in adulthood, but then only in association with
weight increases, not the overall body size of the bird as estimated
through wing or tail lengths (Magaña ). In a smaller sample
of adult males for which we could estimate age, tarsus and cen-
tral toe lengths did not increase with age, unlike wing length or
head length and width (Magaña ). By contrast, central toe
and tarsus in females reach –% of their adult length at age
days and are independent of weight or body size in adult females.
e early juvenile development of central toe and tarsus has most
likely evolved in both sexes through natural selection, to facilitate
running and the rapid weight increase of young in this mainly cur-
sorial species.
Ac k n o w l e d g M e n t s
We are grateful to the farmers in all our study areas for allowing
us to work on their properties. We also thank E. Martín, M. Mo-
rales, and C. Ponce for their collaboration during field work over
several years, H. Litzbarski and T. Langgemach for growth data,
S. Villaverde and M. E. Gómez for a male weight from Albacete,
and two anonymous reviewers for constructive comments on a
previous version of the manuscript. Additional help in the field
was provided by C. Alonso, L. M. Bautista, C. Bravo, H. Bustami,
C. Caldero, A. Correas, J. A. Cruz, E. Fernández, D. González, I. de
la Hera, E. Izquierdo, S. J. Lane, R. Manzanedo I. Martín, C. Mar-
tínez, I. Martínez, R. Muñoz, M. A. Naveso, A. Onrubia, P. E.
Osborne, N. de la Torre, and the guards from Navarra province.
L. M. Bautista helped during RMA analyses. e field work was fi-
nanced by the Dirección General de Investigación (projects PB-
, PB-, PB-, PB-, BOS-, and
CGL-), the Instituto Nacional para la Conservación
de la Naturaleza, and the Direcciones Generales del Medio Natu-
ral of Madrid, Castilla y León and Andalucía. e Consejerías de
Medio Ambiente of the Madrid Community, Junta de Andalucía,
Junta de Castilla y León, Navarra and Aragón, and the provincial
delegations of Toledo and Albacete allowed us to capture birds.
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