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JOURNAL OF AVIAN BIOLOGY 32: 311–318. Copenhagen 2001
The function of female and male ornaments in the Inca Tern:
evidence for links between ornament expression and both adult
condition and reproductive performance
A. Velando, C. M. Lessells and J. C. Ma´rquez
Velando, A., Lessells, C. M. and Ma´rquez, J. C. 2001. The function of female and
male ornaments in the Inca Tern: evidence for links between ornament expression
and both adult condition and reproductive performance. – J. Avian Biol. 32:
311–318.
Inca Terns Larosterna inca are medium-size seabirds that breed along the Peruvian
and Chilean coast. They are monogamous and both sexes incubate and contribute to
chick provisioning. The sexes are similar in appearance and have elaborate orna-
ments, including a long white moustache of feathers and fleshy yellow wattles. In this
paper we report the differences in ornamentation between sexes and examine whether
the trait predicts body condition, reproductive performance or chick quality in either
sex. The ornaments were similar in size and coloration between the sexes, except for
the wattle length, the difference in which can be due to greater head length in males.
Moustache length was the most reliable signal of body condition in both sexes.
Moreover, there was a significant relationship between the moustache length and
reproductive category of adults (non-breeder, unsuccessful breeder, or one or two
chicks fledged). Both asymptotic chick body mass and the T-cell mediated response
of chicks (a measure of immunocompetence) were related to the moustache length of
male and female adults. These results provide support for the role of ornaments in
mutual signalling of condition in this species. Female and male ornaments predict
body condition, reproductive performance and chick quality, as predicted by sexual
selection models.
A.Velando and C.M.Lessells,Netherlands Institute of Ecology,Boterhoeksestraat
48
,
PO Box
40
,
6666
ZG Heteren,The Netherlands.J.C.Ma´rquez,Subdireccio´n de A6es
Marinas,Instituto del Mar del Peru´,Esquina Gamarra y General Valle,Apdo
22
,
Callao-Lima,Peru´ .Present address of A.Velando
:
Departamento de Ecoloxı´a e
Bioloxı´a Animal,Campus Lagoas -Marcosende,Uni6ersidade de Vigo,
36200
Vigo,
Spain.E-mail
:
a6elando@u6igo.es
In many animal species males have elaborate orna-
ments, while females are cryptic in appearance. This
phenomenon has been attributed to sexual selection
acting primarily on the male sex (review in Andersson
1994). Females paired with attractive males may gain
either direct benefits such as territorial resources,
parental care and the avoidance of infectious diseases
(Kirkpatrick and Ryan 1991), or indirect benefits
derived from attractive offspring (Fisher 1930), and
even enhance the viability of their offspring by selecting
traits that indicate male genetic quality (Zahavi 1975,
Hamilton and Zuk 1982, Kodric-Brown and Brown
1984, Grafen 1990). Females can assess the variation in
male quality if males in better condition express more
elaborate display. The idea that male ornaments indi-
cate condition is supported by studies showing that the
expression of ornaments correlates with adult condition
and survival (Andersson 1994). Male ornaments may
also be related to intrasexual selection because they
signal male dominance status (Ja¨rvi and Bakken 1984,
Evans and Hatchwell 1992).
However, females of several species show some ex-
pression of the same ornaments as males. Two main
hypotheses have been proposed to explain this. The
‘correlated response hypothesis’ posits that female or-
naments are themselves selectively neutral or even detri-
mental, but result from a genetic correlation between
the trait in males and females in combination with the
© JOURNAL OF AVIAN BIOLOGY
JOURNAL OF AVIAN BIOLOGY 32:4 (2001) 311
selection for the trait in males (Lande 1980, Muma and
Weatherhead 1989, Hill 1993, Cuervo et al. 1996, Tella
et al. 1997). The ‘direct selection hypothesis’suggests
that female ornaments are themselves under selection,
either through female-female competition or male
choice (Darwin 1871, Jones and Hunter 1999, Amund-
sen 2000). Also female ornaments may signal social
dominance in contests over limited resources, such as
territories or mates (West-Eberhard 1983, Irwin 1994).
Moreover, they may indicate reproductive or genetic
quality, and hence are preferred by choosy males (Jones
and Montgomerie 1992, Johnsen et al. 1996, Potti and
Merino 1996, Amundsen et al. 1997, Linville et al.
1998, but see Hill 1993). Thus, similar preferences for
ornaments in both sexes and similar competition within
both sexes can explain ornament monomorphism in
some bird species (Jones and Hunter 1999).
Mutual sexual preference is expected to occur in
species where members of both sexes benefit from ob-
taining the highest quality mate, such as those where
males provide a substantial amount of parental care to
the offspring (Trivers 1972, Johnstone et al. 1996). In
the Crested Auklet Aethia cristatella, a seabird with
monomorphic ornaments, both sexes showed a prefer-
ence for models with experimentally enlarged crests
(Jones and Hunter 1993). Selection for mutual sig-
nalling of condition is generally expected in seabirds,
because they breed in dense colonies (thus offering
considerable potential for exercising choice), and both
sexes make large contributions to rearing the offspring
and vary substantially in quality (Johnstone et al.
1996). Within both sexes competition can be intense in
seabird species, so intrasexual selection within sexes
could focus on ornaments that function in competition
for access to mates (Jones and Hunter 1999).
Inca Terns Larosterna inca are medium-size seabirds
(c. 220 g) that breed in burrows on talus slopes and
cliffs along the Peruvian and Chilean coast (Guillen
1988). They feed in large flocks on anchovies Engraulis
ringens in the Humboldt current system (Murphy 1936),
and under stable conditions rear two broods in a year.
They are monogamous, pair-formation occurs every
season in the communal areas, and both sexes incubate
and contribute to chick provisioning (Moynihan 1962,
Velando unpubl. data). In other tern species, the total
parental expenditure by males is equal to or outweighs
that of females (Fasola and Saino 1995) and the divorce
rate is very high (c. 58% in Caspian Terns Sterna
caspia, Cuthbert 1985). In Inca Terns the sexes are
similar in appearance, both displaying elaborate orna-
ments including a long white moustache of feathers and
fleshy yellow wattles. The ornaments are displayed dur-
ing the whole year and could be a reliable signal of
quality in both sexes. In this paper we quantified differ-
ences in ornamentation between sexes and examined
whether ornaments predicted body condition, reproduc-
tive performance or chick quality in either sex, as
predicted by some sexual selection hypotheses.
Methods
Study area and studied animals
This study was carried out on the Isla La Vieja,
Reserva Nacional de Paracas, Peru (14°17%S, 76°11%W),
from October to December 1999. Inca Terns build their
nests in crevices in cliffs along the coast of the island
and lay one, or more frequently two eggs. We marked
90 nests in three adjacent sub-colonies during the laying
period. Hatching order and date of hatching of each
chick in the brood were obtained by making daily visits
around the time of hatching. Each chick was tagged
with a coloured velcro strip around the tarsus that
identified chicks within brood. These strips were ex-
panded as the chicks grew. Hatching dates provided an
indication of laying date. The reproductive success of
each nest was recorded as the number of chicks fledged.
During incubation, we captured adults at the nest at
night. To reduce the risk of desertion, we only caught
one adult per nest. Therefore, we could not investigate
assortative mating for ornament size or control for the
ornament size of the other adult in the analysis of
reproductive category. During the same period, we also
captured 16 non-breeding adults by night-lighting at a
roost away from the colonies. Birds were weighed to
the nearest gram using a spring balance. We measured
head length (to the nearest 0.01 mm) with digital cal-
lipers and wing length (to the nearest mm) with a metal
ruler with a stop. A blood sample was obtained from
each bird by puncturing the brachial vein and transfer-
ring the blood to a tube containing an equal volume of
ethanol. Sex was determined through PCR amplifica-
tion of part of the CHD gene using primers P2 and P8
following Griffiths et al. (1998). PCR products were
visualized and photographed under UV light. As ex-
pected, two patterns were observed, one consisting of a
single band of approximately 390 bp, corresponding to
males, and the other showing a second additional band
of approximately 420 bp, corresponding to females. Sex
determined in this way agreed with that based on
behaviour for two females and two males.
Ornament measurements
Inca Terns have slate-coloured plumage and a crimson
bill and legs. They are ornamented with long white
feather moustaches and yellow gape wattles (Fig. 1).
The moustaches consist of tufts of white feathers on
either side of the head running from in front of the eyes
to the back of the cheeks, where they are prolonged by
the plumes of the feathers. We measured the length of
the straightened left and right moustaches of captured
individuals (to the nearest mm) using a transparent
ruler (see Fig. 1). Moustache length was the mean of
these two values, and moustache asymmetry their abso-
312 JOURNAL OF AVIAN BIOLOGY 32:4 (2001)
lute difference. The right wattle length was measured (to
the nearest 0.01 mm) with digital callipers. The colour of
wattles was scored by comparison with a commercial
PANTONE
®
S-5 colour card from 1 (dull orange) to 5
(bright yellow). Birds have a UV-sensitive vision, and
therefore they can perceive colour signals not perceived
by humans (Bennet and Cuthill 1994). This could be a
potential problem for this study because we did not
measure UV-light reflection. Therefore in this study we
may have mis-measured UV colour; however, it has been
argued that quantifying coloration exclusively by human
retina can be reasonable for longer wavelengths (Zuk and
Decruyenaere 1994, Andersson 1999).
Adult condition
We studied the relationships between adult body condi-
tion and ornament expression. In our sample there was
no relationship between body mass and the number of
days between laying and capture dates, so body mass was
not corrected for this variable. In order to avoid the effect
of body size on body condition, we estimated body
condition using residuals from the regression of body
mass (in g) on head length (in mm) for males and females
separately (Females: body mass=4.19 (head length)−
135.89, r
2
=0.19, n=61, pB0.001, Males: body mass =
4.53 (head length)−170.91, r
2
=0.13, n=43, p=0.01).
The residuals were standardized within each sex. We also
carried out the analysis using body mass and the residual
of body mass on wing length (body mass=1.01 (wing
length)−64.23, r
2
=0.12, n=106, pB0.001) as indica-
tors of body condition.
Chick growth and immunocompetence
Asymptotic chick body mass was measured at 25–30
days old using a spring balance (to the nearest gram). As
a measure of immunocompetence, we used the T-cell-me-
diated immune response to an injection of 0.1 mg of
phytohaemaglutinin (PHA) in 0.05 ml of phosphate
buffered saline (PBS) in the left wing web (Smiths et al.
1999). The point of injection was marked with an
indelible marker. Three replicate measurements of
patagium thickness were taken with a digital micrometer
to the nearest 0.001 mm prior to the injection, and again
24 h later. The ‘wing web index’was the change in
thickness (mm) of the wing web (difference between 24-h
post-injection thickness and pre-injection thickness). The
repeatability of wing-web measurements was derived
from the intra-class correlation coefficient (Lessells and
Boag 1987). Wing-web thickness measures were signifi-
cantly repeatable, both for initial measures (r=0.916,
F
58,110
=33.65, pB0.0001) and for final measures (r=
0.959, F
50,102
=70.48, pB0.0001). Asymptotic chick
body mass and wing web index were not related with
chick order, brood size or nestling age, so they were not
corrected for these variables.
Results
Differences between sexes
The mean ornament sizes of adult birds caught during
incubation and sexed by molecular analysis are given in
Table 1. No sexual differences were found in moustache
length, moustache asymmetry and wattle colour. Wattle
length was slightly but significantly longer in males
than in females. Body mass and wing length were
similar in the two sexes, but head length was longer in
males. Moreover, there was a significant correlation
between wattle length and head length (r=0.37, n=
107, pB0.001). Thus, the differences between sexes in
wattle length could be due to sexual differences in head
size.
Relationships among ornament characteristics were
investigated using correlation. Moustache length was
positively correlated with wattle length (r=0.32, n=
104, p=0.001) and wattle colour (r=0.29, n =103
p=0.004). None of the other correlations between
ornament measures were significant (p\0.05).
Ornamentation and condition of adult birds
Body condition (the residuals of body mass on head
size) was related to male and female ornaments (Table
2). Overall, ornaments explained a significant propor-
tion (19%) of the variance in body condition of adult
birds. In analyses of covariance examining sexual dif-
ferences in the relationships between each ornament
measure and body condition, none of the sex or interac-
tion terms were significant (p\0.05 in each case).
Fig. 1. Measurement of Inca Tern ornaments (see Methods).
1. Moustache length, measured to the tip of the longest plume
when the moustache was straightened. 2. Wattle length, mea-
sured as the maximum length of the fleshy wattles.
JOURNAL OF AVIAN BIOLOGY 32:4 (2001) 313
Table 1. Sexual differences in ornaments (see Fig. 1), body size and body mass of adult Inca Terns sexed by molecular analysis
compared by t-tests and Mann-Whitney test. Significant differences are indicated in bold type. Sexual dimorphism index (SDI)
is expressed as male mean/female mean.
Trait Females Males Differences
Mean SE n Mean SE n SDI t or Z
a
p
Head length (mm) 84.27 0.20 62 86.98 0.22 43 1.03 8.85 0.001
Wing length (mm) 280.95 0.82 62 281.02 0.65 43 1.00 0.69 0.94
Body mass (g) 216.9 1.94 62 222.91 2.7 43 1.03 1.78 0.08
1.64 0.6569.67600.5670.37Moustache length (mm) 0.9942 0.46
1.72600.222.03Moustache asymmetry (mm) 0.25 0.410.830.8542
0.17 43 1.04 2.63 0.010.13 15.9815.40Wattle length (mm) 61
2.47Wattle colour score
a
0.240.91400.152.2561 1.15
a
0.10
a
Wattle colour scores were tested using a Mann-Whitney test, for which the Z value is given.
Table 2. Correlation coefficients between body condition (residuals from the regression of body mass on head length for each
sex) and five ornament measures. The results from multiple regression analyses using all trait measures are also shown.
Significant correlations are indicated in bold type.
TotalFemales Males
pr npr nnr p
B0.0011020.380.030Moustache length (mm) 420.330.002600.40
0.166102−0.140.20042−0.200.42560−0.10Moustache asymmetry (mm)
1030.250.049420.29 0.0110.070610.23Wattle length (mm)
Wattle colour score 0.32
a
61 0.011 0.05
a
42 0.741 0.19
a
103 0.052
420.430.013600.44 B0.001102Multiple regression 0.440.080
a
Spearman rank correlation.
Moustache length was the only ornament to which
body condition was significantly related. This variable
accounted for 11% of the variance in male body condi-
tion and 16% of the variance in female body condition.
Similar relationships were found between the residuals
of body mass on wing length, or body mass, and
moustache length (Fig. 2).
There was a significant relationship between mous-
tache length and reproductive category of both sexes of
adults (Fig. 3), but the sex and interaction effects were
not significant. A post hoc analysis (LSD) in both sexes
combined indicated that successful birds had signifi-
cantly longer moustaches than non-breeding ones (p=
0.001). The residuals of moustache length on body
condition (Fig. 2a) were used to control for the effect of
body condition on moustache length. Thus, the effect
of moustache length on reproductive category after
controlling for body condition was also significant
(F
3,86
=2.76, p=0.047). Reproductive category and
success (number of young fledged) were not related to
any other ornament measure (p\0.10 in each case).
Also, there was no relationship between timing of
breeding and any ornament (p\0.10 in all cases).
Adult ornamentation and chick condition
We used body mass and wing web index of chicks as
indicators of chick quality. These measures were
strongly correlated, and therefore nestlings of small
body mass had poorer mean immunocompetence than
those of large body mass (r=0.46, n=27, p =0.01).
Mean chick mass and wing web index were not corre-
lated with parents’body condition (mean chick mass:
r=0.23, n=33, p=0.20; mean wing web index: r =
0.05, n=39, p=0.79). Only parent moustache length
was correlated with mean chick mass and mean wing
web index (Fig. 4). In analyses of covariance examining
sexual differences in the relationships between mous-
tache length and chick mass or immunocompetence
none of the sex or interaction terms were significant
(p\0.05 in each case). Thus, both males and females
with larger moustaches reared heavier chicks with bet-
ter immune responses (Fig. 4).
Discussion
The results of this study showed that ornaments
provide a good indication of individual quality among
adult Inca Terns. Body size, ornament size and col-
oration were similar in both sexes, except for head and
wattle length, which were both longer in males. More-
over, the ornaments provided a similar indication of
condition in both sexes (Table 2). Of the ornaments
measured, moustache length seemed to most reliably
reflect female and male quality: adults with longer
314 JOURNAL OF AVIAN BIOLOGY 32:4 (2001)
Fig. 3. Moustache length (Mean9SE) of adult Inca Terns in
relation to reproductive category. Numbers above the bars are
sample sizes. Because only one adult from each pair was
caught, reproductive category is only scored once for each
nest. The results of General Linear Model (GLM) were: sex:
F
1,82
=0.63, p=0.421; category: F
3,82
=4.67, p=0.005; cate-
gory×sex: F
1,82
=0.34, p=0.797.
Fig. 2. Relationships between body condition (residuals of body
mass on head or wing length) or body mass and moustache
length of adult Inca Terns (44 males, ; and 61 females, ).
moustaches were the most productive and their chicks
were heavier and had better immune responses. These
results are consistent with predictions of honest adver-
tisement models (e.g. Kodric-Brown and Brown 1984,
Grafen 1990). Nevertheless, correlation between orna-
ments and condition may also be consistent with other
models, such as ‘sensory exploitation’(Jones and
Hunter 1998) and ‘Fisherian runaway’(Balmford and
Read 1991, Jones and Hunter 1998). If the ornaments
play an important role in signalling, they may be
involved in mate choice, in competition among mem-
bers of the same sex, or in both (Jones and Hunter
1999, Amundsen 2000).
In many bird species, breeding success declines sea-
sonally (review for seabirds in Moreno 1998) and in
some of these species, the early breeders are more
ornamented (e.g. Ja¨rvi et al. 1987, Møller 1994). In our
study, we did not find any relationship between adult
ornamentation and the timing of breeding. In tropical
seabirds, such as Inca Terns, the timing of breeding is
irregular and not constrained by seasonal influences
(Ashmole 1971, Zavalaga 1997). Thus, a correlation
between ornament expression and laying date is not
expected in this species. We found a positive relation-
ship between chick mass or immunocompetence and
moustache length. However, there was no relationship
between chick mass or immunocompetence and adult
condition, and the relationship between moustache
length and reproductive category was significant also
when controlled for body condition. In Inca Tern
chicks, immunocompetence was positively correlated
with nestling mass. This result agrees with other studies,
which have shown a positive relationship between nu-
tritional condition, survival and immunocompetence of
nestlings (e.g. Saino et al. 1997, Christe et al. 1998; see
JOURNAL OF AVIAN BIOLOGY 32:4 (2001) 315
also Alonso-Alvarez and Tella 2001). In a cross-foster-
ing experiment, cell-mediated immunity in nestling
Great Tits Parus major was due to both environmental
and heritable variation (Brinkhof et al. 1999). Thus, the
correlation between chick mass and immunocompe-
tence and parents’moustache length found in this study
could be due to higher genetic and/or phenotypic qual-
ity of the adults.
There is some indirect evidence that Inca Tern orna-
ments are influenced by sexual selection. Both the white
moustache and yellow wattle appear only in birds of
breeding age. They are prominently emphasized during
courtship and hostile displays in both sexes (Moynihan
1962, Velando unpubl. data), but have no obvious use
in parental care, foraging or thermoregulation. Thus,
the ornaments of Inca Terns may have evolved by
sexual selection driven by mating preferences or intra-
sexual competition.
In several species, there is evidence that ornaments
are the product of sexual selection, but studies have
usually concentrated on male traits (Andersson 1994,
but see Jones and Hunter 1993, 1999, Amundsen et al.
1997, Amundsen 2000, Jones et al. 2000). Studies on
dimorphic birds, in which the females show some lim-
ited expression of the ornaments found in males, have
reached mixed conclusions. Some support the corre-
lated response (Johnson 1988, Muma and Weatherhead
1989, Hill 1993, Cuervo et al. 1996, Tella et al. 1997),
but others support the direct selection hypothesis
(Johnsen et al. 1996, Potti and Merino 1996, Amundsen
et al. 1997, Linville et al. 1998, Hansen et al. 1999).
Few studies have investigated ornament expression in
females of monomorphic species. In Crested Auklets, a
monomorphic seabird, crest size is the product of inter-
and intrasexual selection in both sexes (Jones and
Hunter 1993, 1999, Jones et al. 2000). In Least Auklets
Aethia pusilla, another monomorphic species, there is
also some evidence for mutual sexual selection (Jones
and Montgomerie 1992). Mutual sexual selection (intra-
and intersexual selection) is expected in seabirds be-
cause the parental roles are similar in males and females
(Johnstone et al. 1996, Jones and Hunter 1999) and
many seabird species have sexually monomorphic orna-
ments which are used by both sexes in courtship and
hostile displays (e.g. Inca Tern, Moynihan 1962; trop-
icbirds (Phaethontidae), van Tets 1965; Long-tailed
Skua Stercorarius longicaudus, Andersson 1971; Crested
Auklet, Jones 1993).
Inca Terns are sexually monomorphic in their orna-
ments (Table 1), and we found a significant relationship
between adult condition and ornament expression in
both sexes (Figs 2–3). According to the correlated
response hypothesis female ornaments have no func-
tion, but our results showed a link between female
condition or reproductive performance and the expres-
sion of female moustaches. However, the relationship
between reproductive performance and female orna-
ment could be due to assortative mating with respect to
moustache length and a genetic correlation between
female expression and female preference for male orna-
mentation (Cuervo et al. 1996). In this case, moustache
length should be a better predictor of quality in males
than in females. However, in our study we found
equally strong relationships between reproduction,
chick mass or immunocompetence and ornaments in
females and males. Moreover, the relationship between
ornamentation and condition suggests that ornaments
may be costly to produce or maintain. If the ornaments
are costly, our results agree better with the hypothesis
that female traits are themselves under selection. Orna-
ment expression can be limited by the direct cost of
Fig. 4. Mean wing web index and body mass of nestlings in
relation to moustache length of adult male () and female
() Inca Terns.
316 JOURNAL OF AVIAN BIOLOGY 32:4 (2001)
producing the ornament itself or by social control and
the cost of dominance (Andersson 1994, Jones and
Hunter 1999). During the studied season (October to
December 1999), the terns had a good breeding season
with abundant anchovies, as a consequence of a cold
rich phase after the 1997–1998 El Nin˜o. In 1998, Inca
Terns did not breed due to low anchovy availability
during El Nin˜o (Jahncke 1998). In this year they had
shorter moustaches than in 1999, and there was a
correlation between moustache length and body condi-
tion (explaining 20% of the variance; Velando and
Ma´rquez unpubl. data), which suggests a strong rela-
tionship between ornament expression and adult
condition.
An alternative explanation for the observed relation-
ship between condition and ornament expression, which
we did not test, could be that the ornament expression
is related to age. Age effects would not allow us to
distinguish between correlated and direct hypotheses
(Muma and Weatherhead 1989). In conclusion, our
results seem to support that ornaments have a sig-
nalling function in both sexes of Inca Tern, which is
consistent with the hypothesis that female ornaments
are directly under selection themselves. However, the
correlated response hypothesis cannot be entirely re-
futed by this study, as we did not test whether the
ornaments are used as signals. In addition, this study
provides little insight into which, if any, direct selection
mechanism best explains female ornament function and
evolution. Therefore, experimental studies of this spe-
cies are required to test the role that ornaments play in
signalling parental quality, in mate choice and in intra-
sexual interactions, particularly in females.
Acknowledgements –We are especially grateful to Elisa Goya
for logistic support and to Jose Antonio Godoy and Carlos
Alonso-Alvarez for their help in sexing terns. We also thank
the Instituto del Mar del Peru´(IMARPE), Proabonos and
Intituto Nacional de Recursos Naturales (INRENA) and espe-
cially to Godofredo Can˜ote and Julio Cesar Ruiz for the
permissions to conduct research and for providing facilities on
the Isla La Vieja. During the study, AV was funded with a
grant from Xunta de Galicia, Spain.
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(Recei6ed
30
October
2000
,re6ised
13
March
2001
,accepted
28
March
2001
.)
318 JOURNAL OF AVIAN BIOLOGY 32:4 (2001)
