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Enhanced male coloration after immune challenge increases reproductive potential


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In many animal species, females select a mate on the basis of the expression of secondary sexual traits. A prevalent theory suggests that male ornaments are reliable indicators of immunocompetence, because the cost of immune function prevents cheating. However, sexual signalling is a component of male reproductive effort, and an immune challenge may also alter his perceived future prospects and hence signalling effort. In this study, blue-footed booby males (Sula nebouxii) were inoculated with a diphtheria–tetanus vaccine during courtship to investigate the consequences of mounting an immune response on signalling effort. We found that, after this immune challenge, on average, males increased their signalling effort but lost more body mass compared with control males. Importantly, vaccination affected the partner's reproductive decisions: compared with control females, females paired with vaccinated males laid eggs earlier and increased clutch volume in pairs that laid early. Overall, our results suggest that blue-footed booby males invest more in sexual signals when future breeding opportunities are at risk, eliciting a greater reproductive investment by their partners. Increased signalling effort by infected individuals may contrast the idea of sexual ornaments as signals of infection status.
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Enhanced male coloration after immune challenge increases
reproductive potential
*Departamento de Ecolox
ıa e Biolox
ıa Animal, Universidade de Vigo, Vigo, Spain
Departamento de Ecolog
ıa Evolutiva, Instituto de Ecolog
ıa, Universidad Nacional Aut
onoma de M
exico, M
exico DF, M
female investment;
sexual signals;
terminal investment.
In many animal species, females select a mate on the basis of the expression
of secondary sexual traits. A prevalent theory suggests that male ornaments
are reliable indicators of immunocompetence, because the cost of immune
function prevents cheating. However, sexual signalling is a component of
male reproductive effort, and an immune challenge may also alter his per-
ceived future prospects and hence signalling effort. In this study, blue-footed
booby males (Sula nebouxii) were inoculated with a diphtheriatetanus vac-
cine during courtship to investigate the consequences of mounting an
immune response on signalling effort. We found that, after this immune
challenge, on average, males increased their signalling effort but lost more
body mass compared with control males. Importantly, vaccination affected
the partner’s reproductive decisions: compared with control females, females
paired with vaccinated males laid eggs earlier and increased clutch volume
in pairs that laid early. Overall, our results suggest that blue-footed booby
males invest more in sexual signals when future breeding opportunities are
at risk, eliciting a greater reproductive investment by their partners.
Increased signalling effort by infected individuals may contrast the idea of
sexual ornaments as signals of infection status.
In iteroparous organisms, resources allocated into cur-
rent reproduction reduce future reproductive prospects;
therefore, individuals commonly restrict their current
effort to maximize lifetime success (Curio, 1983;
Stearns, 1992). In many species, male reproductive suc-
cess depends on the expression of sexually selected
traits (Andersson, 1994), which often are costly to pro-
duce and maintain (Kotiaho, 2001; Maynard-Smith &
Harper, 2003; Cotton et al., 2004). Thus, sexual signal-
ling is a component of reproductive effort (Getty,
2006), and the amount of resources invested into cur-
rent sexual advertisement probably results in reduced
residual reproductive value (Kokko, 1997; Hunt et al.,
2004; Getty, 2006). Hence, optimal sexual signalling
effort will depend on both future breeding opportuni-
ties and current probabilities of success (Lindstr
et al., 2009).
A prevalent theory of sexual selection suggests that
ornaments honestly reflect the individual’s genetic abil-
ity to resist parasites and pathogens (Hamilton & Zuk,
1982; Folstad & Karter, 1992). Parasites and pathogens
are likely to be one of the major extrinsic causes of
mortality among wild animals (Grenfell & Dobson,
1995). Infectious organisms activate immune defences
of hosts (Pastoret et al., 1998), and this activation is
energetically costly and induces oxidative stress
(reviewed in Hasselquist & Nilsson, 2012). Immune up-
regulation diverts resources from other functions such
as sexual signals (Faivre et al., 2003; Alonso-Alvarez
et al., 2004; Garamszegi et al., 2004; Peters et al., 2004;
Fitze et al., 2007; Cote et al., 2010). Costs associated
with immune activation can prevent ‘cheating’ because
only superior healthy males may be able to produce
elaborate ornaments. Furthermore, current evidence
suggests that activation of the immune system may cue
organisms about the risk of infections that threaten
Correspondence: Alberto Velando, Departamento de Ecolox
ıa e Biolox
Animal, Campus As Lagoas, Universidade de Vigo, 36310 Spain.
Tel.: +34 986812550; fax: +34 986812556; e-mail:
Present address: Centro Tlaxcala de Biolog
ıa de la Conducta,
Universidad Aut
onoma de Tlaxcala, Tlaxcala, M
doi: 10.1111/jeb.12416
future survival and reproduction (Moret, 2003; Bon-
neaud et al., 2004; Velando et al., 2006a). According to
life history theory, individuals with declining future
reproductive prospects should increase their investment
in current reproduction (Williams, 1966; Pianka & Par-
ker, 1975; coined as ‘terminal investment’, Clutton-
Brock, 1984). Thus, paradoxically, infected individuals
might increase their signalling effort (i.e. dishonestly
signalling their infection status; Polak & Starmer, 1998;
Sadd et al., 2006; Nielsen & Holman, 2012; Copeland &
Fedorka, 2012).
Signalling effort may be strategically adjusted espe-
cially in labile sexual traits, such as song rate or colour
in integuments. In many monogamous species, these
labile traits continue to be exhibited after pair formation
(see Torres & Velando, 2003, 2010), and it has been sug-
gested that the presence of ornaments after pairing
might stimulate partner investment (Wachtmeister,
2001; Servedio et al., 2013). In species with biparental
care, there is potential conflict between male and female
parents over how much parental investment each
should provide (sexual conflict; Lessells, 1999). Dynamic
signals indicative of current reproductive effort are
expected to evolve as signalling strongly affects the
negotiation between mates over offspring care (McNa-
mara et al., 1999; Morales et al., 2009). Thus, in species
with biparental care, high investment in signalling prob-
ably increases partner contribution to current reproduc-
tion (Velando et al., 2006b), at the cost of reducing
future breeding opportunities (Candolin, 2000a).
The blue-footed booby (Sula nebouxii), a long-lived
socially monogamous seabird, is a good model species
to examine the effect of immune activation on male
signalling effort and partner’s breeding response. In this
species, parental effort is high, both parents incubate
and feed the chicks for a long period (up to 145 days;
Torres & Drummond, 1999; Guerra & Drummond,
1995), and the probability of success depends on the
partner contribution to brood care (Velando & Alonso-
Alvarez, 2003). After pairing, there is an extended
courtship period (up to 40 days; Osorio-Beristain &
Drummond, 1998), which probably serves for partner
evaluation (Torres & Velando, 2010). Males (especially)
have conspicuous and variably coloured feet that are
exhibited prominently during pair courtship (Nelson,
1978; Torres & Velando, 2010).
In this species, foot colour varies from bright blue
green to dull blue as a result of the combined effects of
collagen arrays and carotenoid pigments (Velando et al.,
2006b). Females prefer males with greener feet (Torres
& Velando, 2003, 2010), which result from high carot-
enoid deposition into foot integument (Velando et al.,
2006b; Torres & Velando, 2010). Several experimental
studies suggest that the mate signalling effort (i.e. carot-
enoid deposition) affects female courtship and copula-
tion rates and reproductive decisions (Torres &
Velando, 2003; Velando et al., 2006b; Dentressangle
et al., 2008; see Torres & Velando, 2010). As carote-
noids have antioxidant and immunomodulatory proper-
ties (Blount et al., 2003; McGraw & Ardia, 2003),
individuals should optimize pigment allocation into
integuments according to the trade-off between physio-
logical requirements and reproductive benefits.
In this study, we inoculated blue-footed males with
nonpathogenic antigens (diphtheriatetanus vaccine)
early in the courtship period to investigate the conse-
quences of mounting an immune response on signal-
ling effort (foot colour) and the partner’s reproductive
responses. The diphtheriatetanus vaccine activates the
immune system in birds without inducing the negative
effects of pathogens (Svensson et al., 1998; R
aberg et al.,
2000). In birds, the acute phase of immune activation
lasts a few days and the physiological responses proba-
bly end within 2 weeks (Svensson et al., 1998; Verhulst
et al., 2005). The acute phase of an immune response
leads to diversion of resources to combat immediate
and unavoidable physiological costs (see Hasselquist &
Nilsson, 2012). After injection, we recaptured males
during the expected duration of physiological responses
(911 days) and again later during early incubation,
likely sufficient time to allow recovery from the physio-
logical costs of mounting a defence (Verhulst et al.,
We expected that the negative effects of immune
activation on male coloration (if any) will be evident at
first recapture, when carotenoids are needed to palliate
the cost of immune up-regulation (Torres & Velando,
2007). In contrast, if immune activation is a cue to the
risk of infection and declining reproductive prospects
(Bonneaud et al., 2004; Velando et al., 2006a), immu-
nologically challenged males may increase their signal-
ling effort (Sadd et al., 2006) to motivate the partner’s
contribution to current reproduction (Torres & Velando,
2010). Thus, we also studied reproductive responses
(laying probability, laying date and clutch investment)
of females paired with vaccinated males.
Materials and methods
The study was carried out in the breeding colony of the
blue-footed booby Sula nebouxii at Isla Isabel (21°520N,
105°540W), Nayarit, Mexico, from January to March
2004. In January, 40 paired courting males were cap-
tured and randomly assigned to the experimental or
control treatments (n=20 in each treatment). Males
were captured during two consecutive nights (January
89), on average 29 days before laying (range 17
49 days). The birds were captured and manipulated at
night to reduce disturbance. Males were ringed with a
numbered metal ring and marked by painting a black
spot on the neck (with a nontoxic marker) to facilitate
resighting and future recaptures. Experimental
males were injected in the pectoral muscle with 200 lL
of diphtheriatetanus vaccine (Ditantrix vaccine,
ª2014 THE AUTHORS. J. EVOL. BIOL. doi: 10.1111/jeb.12416
GlaxoSmithKline, Madrid, Spain; diphtheria toxoid
8 IU and tetanus toxoid 0.8 IU mixed with aluminium
hydroxide at 3.0 mgmL
and 0.9% NaCl solution).
Control males were injected with an identical volume
of 0.9% NaCl solution. The diphtheriatetanus vaccine
contains two toxoid antigens novel to the birds, so the
effects are only derived from activating the host
humoral immune defence system (Svensson et al.,
1998; Ilmonen et al., 2000). Nest sites were inspected
daily until the eggs were laid. On the laying day, eggs
were marked with a pencil, and their length (L) and
width (W) were measured (accuracy 0.1 mm) to calcu-
late egg volume (V =0.51LW
; Hoyt, 1979). Overall, 29
females paired with focal males laid eggs (see Results).
Nine to eleven days after manipulation (hereafter
10 days), 30 males were recaptured (14 control and 16
experimental), and then during the first 2 weeks of
incubation, 24 incubating males were again recaptured
(11 control and 13 experimental). In the three capture
events (prior to manipulation, first recapture [10 days
later] and second recapture [during incubation]), birds
were weighed and their foot colour was determined by
taking three measurements on the foot web using a
spectrophotometer that analyses the reflectance spec-
trum from 360 to 740 nm wavelength at 10-nm inter-
vals (MINOLTA CM-2600d, Minolta Co. Ltd, Osaka,
Japan). From the foot-colour spectrum, we calculated
green chroma as the proportion of reflectance between
460 and 620 nm (the range of highest visual sensitivity
in blue-footed boobies; Reed, 1987; Velando et al.,
2006b). In this species, males displaying greener feet
during courtship are more attractive to females (Torres
& Velando, 2003, 2010; Velando et al., 2006b).
Prior to the manipulation, foot colour and body mass
of males did not differ between treatments (green
chroma, t
=0.11, P=0.91; body mass, t
P=0.25). Changes in foot colour and body mass with
respect to the initial state (i.e. difference between the
values at recaptures after vaccination and initial values)
were analysed by mixed linear models (Littell et al.,
1996). The model included individual birds as subject
factor, the vaccination treatment as between-subject
factor, and the repeated measures at different recapture
events (i.e. first and second recapture) as within-subject
factor. The interaction between treatment and recap-
ture event was included in the models but removed
when nonsignificant.
The probability to establish a clutch and laying date
(Julian day) was analysed using generalized linear
models with binomial error distribution and a logit link
function and a Poisson error and log link, respectively.
The models included vaccination treatment as factor
and green chroma during courtship (initial capture and
first recapture event) as covariates. Clutch volume
(sum of volume of all eggs), a proxy of female invest-
ment (Morales et al., 2009), was analysed using a gen-
eral linear model that included vaccination treatment
as a factor, and laying date, and male green chroma
and body mass during incubation as covariates; two-
way interactions between covariates and treatment
were also tested. Models were simplified by backward
deletion procedure starting with two-way interaction
effects. Results are presented as means standard
error, and the significance level was set at 0.05.
Change in body mass and foot colour
Vaccination treatment strongly influenced body mass
loss (F
=7.85, P=0.009). Vaccinated males lost, on
average, 10% of body mass, whereas control males lost
2.5% (Fig. 1a). Body mass change did not differ
between recapture events (F
=0.17, P=0.68), and
Change in body mass (g)
Change in green chroma
First recapture
Second recapture
Fig. 1 Effects of diphtheriatetanus vaccination on males (open
bars represent control males and closed bars vaccinated males)
recaptured during courtship (911 days after vaccination, n=30
males) and during the first two weeks of incubation (1741 days
after vaccination, n=24 males) on the change in (a) body mass
and (b) green chroma. Values are expressed as the difference
between recapture and initial values.
ª2014 THE AUTHORS. J. EVOL. BIOL. doi: 10.1111/jeb.12416
Signalling effort after immune challenge 3
the interaction between recapture event and treatment
was not significant (F
=0.01, P=0.95).
Foot colour changed to duller blue as the season pro-
gressed (F
=4.37, P=0.049; Fig. 1b). Vaccination
had a significant effect on mean change of foot colour
=6.37, P=0.017). Thus, green chroma faded on
average 2.5% in control males, but only 0.76% in vac-
cinated males (Fig. 1b). In the last (second) recapture,
none of the vaccinated males lost more than 2.5% of
initial foot colour, yet 54% of control males lost more
than 4% of initial colour. The interaction between
recapture event and treatment was not significant (F
=1.17, P=0.29).
Reproduction and partner investment
From 40 males initially captured during the courtship
period, only 29 (73%) established a clutch. Initial green
chroma influenced the probability of laying (v
P=0.037). Greener males prior to vaccination were
more likely to establish a clutch (Fig. 2). Treatment did
not influence the probability of reproduction (v
P=0.71). In those males that established a clutch, vac-
cinated males established a clutch 4.8 3.0 days earlier
than control males (v
=4.56, P=0.033; Fig. 3). Green
chroma before vaccination did not influence laying date
(P>0.10 in all cases).
Clutch volume was affected by the interaction
between treatment and laying date (F
P=0.049). Females paired with vaccinated males laid
larger clutches than control males, but only in pairs that
laid early (Fig. 4a). Green chroma in the first recapture
had a positive effect on clutch volume (F
P=0.030). Thus, females paired with more colourful
males increased investment in the clutch (Fig. 4b).
We found that, on average, vaccinated males lost more
body mass but maintained greener foot colour com-
pared with control males. Experimental males increased
their signalling effort after an immune challenge, prob-
ably because infection is a cue of declining reproductive
prospects (Bonneaud et al., 2004). Importantly, an
immune challenge on males affected the partner’s
0.5 0.51 0.52 0.53 0.54
Probability to establish a clutch
Green chroma
Fig. 2 Probability to establish a clutch according to foot green
chroma of males (n=40) captured during early courtship (initial
premanipulation capture).
Laying date (julian day)
Control Vaccinated
Fig. 3 Effect of diphtheriatetanus vaccination on laying date of
males that established a clutch (n=29).
Laying date
Early Late
0.49 0.5 0.51 0.52 0.53 0.54
Green chroma
Clutch volume (cm
Clutch volume (cm
Fig. 4 Female investment measured as clutch volume (cm
according to (a) vaccination treatment (open circles: control males;
closed bars: vaccinated males) and laying date (for illustrative
purposes, laying date was categorized in early and late according
to mean laying date); (b) green chroma of males in the first
recapture (courtship period; n=24).
ª2014 THE AUTHORS. J. EVOL. BIOL. doi: 10.1111/jeb.12416
reproductive decisions. Compared with control females,
females paired with vaccinated males laid eggs earlier,
and clutch volume was increased in early laying pairs.
Overall, these results suggest that by enhancing foot
coloration, vaccinated males induced a greater repro-
ductive investment from their partners. Thus, blue-
footed booby males invest more in sexual signals when
future breeding opportunities are at risk, enhancing
their current probabilities of breeding success.
In our study, courting blue-footed booby males were
immunologically challenged with diphtheria and teta-
nus toxoids. The acute phase after vaccination typically
lasts a few days and is characterized by a systemic
inflammatory response (Sorci & Faivre, 2009; Sorci,
2013). The second phase is the activation of humoral
immunity, with a peak response within 2 weeks (e.g.
Svensson et al., 1998). Immunized blue-footed booby
males lost more body mass 911 days after vaccination
(i.e. at first recapture, during the physiological
response) than saline injected males, a difference in
body mass that remained at least until the first 2-weeks
of incubation. Body mass decrease of immune-chal-
lenged males might result from energetic costs of
mounting an immune response (e.g. Ots et al., 2001).
Nevertheless, we cannot exclude the possibility that
body mass decline of vaccinated males resulted from
reduced feeding rates (e.g. Bonneaud et al., 2003;
reviewed in Hasselquist & Nilsson, 2012), or increased
mating effort.
According to theory, when male ornaments are reli-
able indicators of infection status, an immune challenge
should reduce the expression of sexual signals (Hamil-
ton & Zuk, 1982). Contrary to this prediction, in our
study, immunization did not reduce male coloration by
the time of the first recapture, when carotenoids were
expected to have been mobilized to palliate the cost of
immune activation (Torres & Velando, 2007). Instead,
we found that immunized males maintained greener
feet than control males, and this difference was more
pronounced at the second recapture, after the acute
phase of immune activation, roughly a month after
vaccination. Previous studies on birds have found that
an immune challenge resulted in the reduced expres-
sion of carotenoid-dependent bill colour (Faivre et al.,
2003; Alonso-Alvarez et al., 2004; Peters et al., 2004;
Cote et al., 2010). It is possible that context-dependent
effects and differences in the experimental procedure
(e.g. recapture time, doses, antigen used) might explain
the discrepancy between these studies and our results.
Interestingly, in all of these studies, males were main-
tained in captivity with no access to females, whereas
in our study, birds were only captured for a few min-
utes in their natural environment. Animals are
expected to maximize reproductive effort, so maintain-
ing costly carotenoid-dependent coloration may not be
the best strategy when the chances of reproduction are
low. Additionally, differences in other life history traits
such as patterns of parental care and age-dependent
variation in optimal allocation of resources to the
immune function and reproduction might explain some
of the variability among studies (e.g. Cote et al., 2010).
In a previous study, we found that blue-footed booby
middle-aged males, but not senescent males, were able
to maintain their foot colour 1 week after immune acti-
vation, during the acute phase (Torres & Velando,
2007). Overall, our results suggest that, with the excep-
tion of senescent males that are probably physiologi-
cally limited, blue-footed booby males maintain
colourful feet during several weeks after the acute
phase of an immune challenge.
Carotenoid supplementation in blue-footed boobies
increases immune function and foot colour (Velando
et al., 2006b; Beamonte-Barrientos et al., 2014), sug-
gesting that these pigments are a limiting factor for
both functions. As carotenoid-dependent integuments
continuously demand carotenoid pigments (Alonso-
Alvarez et al., 2004), our results suggest that immu-
nized males prioritized reproductive effort over other
functions. For blue-footed booby males, continuous
allocation of carotenoids to foot colour during courtship
may influence the probability of being cuckolded (Tor-
res & Velando, 2003) and female reproductive decisions
(Torres & Velando, 2010). Thus, vaccinated males prob-
ably increased their signalling effort to improve their
current reproductive success.
The increased signalling effort of vaccinated males
suggests that pathogen exposure changed their life his-
tory strategy. Activation of the immune system is an
important cue to the risk of infections that may threa-
ten survival (Bonneaud et al., 2004). When perceived
future prospects are low, for example after a pathogen
threat, organisms should increase their reproductive
effort (Williams, 1966; Clutton-Brock, 1984). Accord-
ingly, several studies have documented an increase in
reproductive effort after experimental activation of the
immune system (e.g. Bonneaud et al., 2004; Hanssen,
2006; Velando et al., 2006b; Weil et al., 2006; Bowers
et al., 2012). An increase in sexual advertisement after
an immune challenge has also been reported in three
invertebrate species (Polak & Starmer, 1998; Sadd et al.,
2006; Copeland & Fedorka, 2012; Nielsen & Holman,
This life history strategy has potentially important
implications for the evolution of sexual signals. Sexual
signalling effort depends on the trade-off between cur-
rent reproduction and future breeding opportunities
(Getty, 2006). Infected individuals, with low future
prospects, may increase their effort to improve their
current probabilities of mating (Kokko, 1997; Candolin,
2000b; Lindstr
om et al., 2009). In Drosophila nigrospira-
cula, experimentally parasitized males increased their
courtship rate but lived shorter than unparasitized con-
trol males (Polak & Starmer, 1998). In species with no
parental care, potential sexual conflict arises because
ª2014 THE AUTHORS. J. EVOL. BIOL. doi: 10.1111/jeb.12416
Signalling effort after immune challenge 5
females may pay a cost when mating with more orna-
mented males that display increased investment in sex-
ual signalling after an infection (e.g. Sadd et al., 2006;
Copeland & Fedorka, 2012). In species with parental
care, female response to mate signalling effort by
infected individuals might be adaptive if signalling
effort also correlates with parental effort.
Our results indirectly show that female reproductive
decisions depended on mate’s coloration. In a previous
study, we found that males with colourful feet early in
the courtship period were paired with high-quality
females, in terms of body condition (Torres & Velando,
2003). Accordingly, in the present study, males with
greener foot colour in the first capture (prior to experi-
mental manipulation) had greater probabilities to estab-
lish a clutch, suggesting that foot colour influences
mate choice. Nevertheless, female breeding decisions do
not end at pairing. In our experiment, females paired
with vaccinated males laid earlier in the season and laid
larger clutches early in the season compared with
females paired with control males. Both of these life
history traits, laying date and egg investment have a
strong impact on fitness in the blue-footed booby
(Drummond et al., 2003; D’Alba & Torres, 2007; Torres
et al., 2011). Furthermore, our present results confirm
previous experimental studies. During the egg laying
period in three different years, when male coloration
was modified to a duller blue, females consistently
responded by reducing second-egg volume (Velando
et al., 2006b; Dentressangle et al., 2008; Torres & Velando,
2010). Hence, increased signalling effort of vaccinated
males probably led to an increase in reproductive invest-
ment by females.
In many species, females use male ornaments to
adjust their current investment (Horv
aet al.,
2012). As it is thought that male sexual signals indicate
male genetic quality, this flexible strategy has been
traditionally explained as an adaptive adjustment to the
expected returns on investment (i.e. differential alloca-
tion hypothesis; Burley, 1988; Sheldon, 2000). Further-
more, in species with biparental care, negotiation
models suggest that females may adaptively adjust their
current investment depending on their partner’s contri-
bution (Lessells & McNamara, 2012). Additionally,
displays after pair-bond formation might evolve essen-
tially to stimulate partner’s investment in offspring,
often leading to cooperation (Servedio et al., 2013). In
the blue-footed booby, previous studies suggest that
females adjust their reproductive investment according
to parental ability of their mates (Velando & Alonso-
Alvarez, 2003; Torres & Velando, 2010). Importantly,
offspring condition strongly correlates with father’s foot
colour during chick rearing (Velando et al., 2005), sug-
gesting that foot colour may be indicative of parental
effort. Overall, this experimental study, together with
previous results (Torres & Velando, 2010), reveals the
existence of a mechanism mediated by sexual signals to
fine-tune communication between mates over parental
care (see also Morales et al., 2012); whether this
exchange of information results from sexual conflict or
stimulation remains to be studied.
In conclusion, this study found that immune-chal-
lenged males increased their signalling effort, thus
enhancing female investment in current reproduction.
The existence of enhanced sexual advertisement by
infected males challenges the generality of the long-
lasting idea of sexual ornaments as signals of parasite
resistance (Hamilton & Zuk, 1982; Folstad & Karter,
1992). Sexual signals and female responses are compo-
nents of reproductive investment of individuals subject
to complex life history tradeoffs (Kokko, 1997; Getty,
2006; Lindstr
om et al., 2009). Manipulation, coopera-
tion or negotiation scenarios should be explored by
future studies to disentangle the persistence of
enhanced signalling exhibited by immunologically chal-
lenged individuals.
Logistic support was provided by the staff from the Par-
que Nacional Isla Isabel and the fisherman from San
Blas and Camichin. We are grateful to Christoph Haag,
Andreanna Welch and two anonymous reviewers for
comments on the manuscript. The study was supported
by UNAM (IN230603, IN211406), CONACYT (47599)
and the Spanish Ministerio de Ciencia e Innovaci
(CGL2006-10 357-C02-01 and CGL2012-40229-C02-
02). The authors declare that they have no conflicting
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... 61 The highest investment in reproduction under unfavorable conditions, as we have observed in the Pb exposed females, has been explained by mechanisms defined as "terminal investment" 63 or reproductive compensation. 62,64 In the case of the terminal investment, Velando et al. 63 observed that immunologically challenged bluefooted booby males (Sula nebouxii) increased their signaling effort but lost body mass, which affected the partner's reproductive decisions (e.g., earlier laying and increased clutch volume). These authors 63 suggest that males invest more in sexual signals when future breeding opportunities are at risk, eliciting a greater reproductive investment by their partners. ...
... 62,64 In the case of the terminal investment, Velando et al. 63 observed that immunologically challenged bluefooted booby males (Sula nebouxii) increased their signaling effort but lost body mass, which affected the partner's reproductive decisions (e.g., earlier laying and increased clutch volume). These authors 63 suggest that males invest more in sexual signals when future breeding opportunities are at risk, eliciting a greater reproductive investment by their partners. Similarly, the hypothesis of reproductive compensation predicts that reproduction under constrains results in an increased parental reproductive effort and investment in offspring (e.g., enhanced female fecundity, greater egg size and increased male sperm number per ejaculate) to ensure its viability, but individuals that compensate have lower survival probabilities. ...
Lead (Pb) poisoning via ingestion of shot pellets is a frequent cause of death in wild birds and also has a wide range of subclinical effects. Here we report on the sublethal effects Pb exposure has on the breeding performance of red-legged partridges (Alectoris rufa). We studied the effects of Pb exposure on sperm quality, reproductive success, egg properties, laying performance, antioxidants levels and carotenoid-based colouration. Birds were exposed by oral gavage to one or three No. 6 Pb shot pellets (2.8 mm in diameter, mean mass ± SD: 109 ± 7.97 mg). We show that exposure to 3 pellets (330 mg) reduced the hatching rate of females and decreased the acrosome integrity and sperm motility of males. In addition, females exposed to 1 pellet (110 mg) produced heavier eggs and chicks, whereas males exposed to 1 pellet presented an increase in sperm vigour. Sperm viability, concentration, progressiveness or fecundation rate were not affected by Pb treatment. Pb exposure increased circulating antioxidant levels in males, whereas the percentage of carotenoid-pigmented eye-ring area decreased in exposed females. Several sperm parameters showed positive relationships with colouration and antioxidant levels, suggesting that males displaying redder ornaments may be more capable of protecting sperm from oxidative stress in the event of sublethal Pb exposure.
... This may be because females are more vulnerable to oxidative stress than males (Vallverdú-Coll et al. 2016) and because allocation of carotenoids to the egg yolk occurred in order to protect the embryo from oxidative stress (Pérez-Rodríguez 2008). This would tend to increase offspring survival prospects at the expense of the female´s own oxidative balance (Velando et al. 2014). Although lead exposure has been predominantly associated with less coloured birds in these studies, in some scenarios carotenoid-based coloration has increased rather than decreased after lead exposure. ...
... Significantly, it is possible that some of these effects were mediated by female responses to male infection status. In a second study, blue-footed booby males received either a diphtheria-tetanus vaccine or a control injection during courtship (Velando et al., 2014). The female partners of these males laid eggs earlier and their earlier clutches had larger volume (sum volume of all eggs). ...
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1. Uninfected animals can attempt to prevent parasitism in many ways. Behavioral avoidance of parasitized conspecifics, for instance, is documented in several species. 2. Interactions with parasitized conspecifics can also, however, lead to physiological changes in uninfected animals, an effect that is much less well studied, and consequently, less well understood. The way in which exposure to parasitism risk changes the physiology of uninfected animals and the impacts of those changes on animal fitness remain a significant gap in knowledge. 3. Determining how the disease environment experienced by animals impacts their physiology, survival, and reproduction, has major implications for our knowledge of how parasites affect populations beyond their consumptive effects. If the physiological changes triggered in uninfected animals help reduce disease burden or speed up recovery from disease, they can have cascading effects on disease dynamics; therefore, they are important to study and understand. 4. In this Perspective, I highlight studies in vertebrates and invertebrates that demonstrate the existence of these responses. I also consider how these responses may be adaptive and instances when they should occur. Finally, I briefly discuss the importance of studying these responses in relation to animal welfare, human health, disease dynamics, and experimental design.
... Our results showed that less ornamented and more parasitized grassquit males (i.e., low residual reproductive value) were able to perform sexual displays that are as intense as those performed by fully ornamented and healthier males in high predation risk contexts. Therefore, our data agree with one of the key predictions of the terminal investment hypothesis (Williams 1966;Trivers 1972;Pianka and Parker 1975): individuals with low residual reproductive value (i.e., reduced expectations of future reproduction) should increase their current reproductive effort when facing a high perceived risk of extrinsic mortality (Velando et al. 2006(Velando et al. , 2014Copeland and Fedorka 2012;Nielsen and Holman 2012). ...
Sexual signaling coevolves with the sensory systems of intended receivers; however, predators may be unintended receivers of sexual signals. Conspicuous aerial displays in some species may place males at high risk of predation from eavesdropping predators. There are three different hypotheses to explain how signaling males can deal with increased predation risk: (1) males invest in survival by decreasing signal conspicuousness; (2) males invest in reproduction by increasing signal conspicuousness; and (3) male response is condition-dependent according to his residual reproductive value. Here, we used blue-black grassquits (Volatinia jacarina) to test these hypotheses, asking whether males modify leap displays under different levels of predation risk. Grassquit males develop an iridescent nuptial plumage and spend considerable time emitting a multimodal signal: while leaping from a perch, males clap their wings above their heads and emit a high-pitched short song. We exposed males to predator and nonpredator playbacks while video recording their displays. We found interactions between predation risk and 2 male condition variables (ectoparasite infestation and proportion of nuptial plumage coverage) that influenced display behavior. Less parasitized males and those with higher proportion of nuptial plumage showed no change in display behavior, while more parasitized males and those with lower proportion of nuptial plumage increased the vigor of displays under predation risk. In other words, males with low residual reproductive value increased reproductive effort when there was a high risk of extrinsic death. Our study provides some empirical support for the terminal investment hypothesis.
... Although the proximate mechanisms linking health to ornamentation are increasingly well explored, evidence that infection in natural populations is revealed by sexually selected traits continues to be mixed (Møller et al. 1999;Griffith and Pryke 2006). While parasitized males produce relatively dull or less elaborate ornaments in some species (Hill and Farmer 2005;Lumpkin et al. 2014;Balenger et al. 2015), in others, ornamentation and display behaviors appear to be unrelated to a male's infection status (Dufva and Allander 1995) or even positively related to parasite burden (Trigo and Mota 2016) or current/prior immune activation (Velando et al. 2014). ...
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Although the selective loss of individuals susceptible to disease can favor the evolution of female preference for older males, the interrelationship between age, infection, longevity, and mating success remains poorly characterized in natural populations. In a longitudinal study of 61 male common yellowthroats (Geothlypis trichas), we found that the probability of infection with hematozoa increased as males aged from 1 to 5 years. Despite a significant, negative association between infection and longevity that partially masked age-effects, the odds that a male was infected with Trypanosoma, Plasmodium, or Leucocytozoon increased 71–212% per year. Nearly 75% of males in their first breeding season were either uninfected or infected with only a single parasite, while 50% of older males were infected with at least two parasites and 16% were infected with all three. No males escaped infection after their second breeding season. Older males were also more likely to sire extra-pair young (EPY) and, as a consequence, infection with multiple parasites was associated with a fourfold increase in the odds of producing EPY. Unlike younger males, 80% of the oldest males had a history of either surviving chronic infection or recovering. Combined with previous work showing higher diversity at the major histocompatibility complex among older males, our results suggest that the song and plumage traits that signal male age in common yellowthroats also, perforce, signal resistance to parasites. By preferring older males, females may obtain good genes for disease resistance even in the absence of any effect of infection on male ornamentation.
... Environmental toxins can disrupt carotenoid bare-part coloration within 1 mo (Bortolotti et al. 2003, Pérez et al. 2010a, 2010b, and challenges to both the innate and acquired immune system typically result in duller carotenoid bare parts within days or weeks (Faivre et al. 2003a, Alonso-Alvarez et al. 2004, Peters et al. 2004a, Gautier et al. 2008, Rosenthal et al. 2012; but see Velando et al. 2014). Carotenoid bare parts may respond rapidly (within 6.5 hr) to stressors, including capture and captivity (Rosen and Tarvin 2006, Biard et al. 2009, Sternalski et al. 2010, Rosenthal et al. 2012, Vergara et al. 2015, and their color reflects indices of recent stress such as corticosterone levels or the heterophil:lymphocyte ratio (Roberts et al. 2007, Pérez-Rodríguez and Viñuela 2008, López et al. 2011, Kelly et al. 2012. ...
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Avian plumage has captivated scientists and the public alike for generations and has been a fundamental study system for research into signal evolution. By contrast, relatively little attention has been paid to avian bare parts such as exposed skin, bills, feet, and combs, despite considerable variation in structure and coloration within and between species. To better understand the potential signaling role of bare parts, we conducted a comprehensive literature search that returned 321 published studies. In reviewing these studies, we found that (1) bare-part color is widely distributed taxonomically and is produced by diverse mechanisms; (2) many bare parts are likely to be dynamic, honest signals of current condition or status and can also reflect genetic makeup and early developmental conditions; and (3) bare parts can function as pluripotent social signals, mediating interactions between competitors, mates, and kin. Differences between bare parts and plumage in phenology and information content support a multiple-messages interpretation of their respective signaling roles, in that bare parts may contain information that is complementary to, but distinctive from, information conveyed by plumage-based signals. We consider it likely that a great deal of barepart variation is ‘‘hidden in plain sight,’’ in that meaningful variation may not be recorded by many current studies. We urge more careful and extensive characterization of bare-part coloration in a wider range of species because of its potential to advance our understanding of signal function and constraints, with particular reference to the role of dynamic color signals and the evolution of multiple ornamentation.
... Parasites drain resources (including pigments and nutrients) from their hosts, which might otherwise be partly allocated to producing ornaments. Furthermore, in fighting parasites, hosts also mount immune responses that divert resources from other functions such as ornamentation (Rosenthal et al. 2012;Velando et al. 2014). Regardless of the underlying mechanism, parasitism should Figure 5 Changes in yellow-orange beak chroma (YO chroma ) in 20 male king penguins (Aptenodytes patagonicus) that endured a prolonged fast in captivity. ...
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Dynamic ornamental signals that vary over minutes, hours or weeks can yield continuous information on individual condition (e.g., energy reserves or immune status), and may therefore be under strong social and/or sexual selection. In vertebrates, the coloration of the integument is often viewed as a dynamic ornament, which in birds can be apparent in the beak. King penguins (Aptenodytes patagonicus) are monomorphic seabirds that possess conspicuous yellow–orange (YO) and ultraviolet (UV) beak spots that are used by both males and females in mate choice. We studied the dynamicity of beak spot sexual traits, and to what extent they reflected changes in individual condition in fasting king penguins and in penguins treated with an anti-parasitic drug. We also describe the maturation of this colorful ornament during the yearly catastrophic moult. On a time-scale of days to weeks, beak spot coloration changed in response to fasting and experimental changes in parasite load. Beak spot UV brightness decreased over a 10-day fast in breeding birds. For birds caught during courtship and held in captivity YO chroma decreased after a 24-day fast. Birds that were treated with an anti-parasitic solution showed an increase in UV coloration after parasite removal. Altogether, our results show that beak spot coloration is a dynamic ornament that reflects multiple dimensions of changes in individual condition in breeding-fasting penguins.
When animals are sick, their physiology and behavior change in ways that can impact their offspring. Research is emerging showing that infection risk alone can also modify the physiology and behavior of healthy animals. If physiological responses to environments with high infection risk take place during reproduction, it is possible that they lead to maternal effects. Understanding whether and how high infection risk triggers maternal effects is important to elucidate how the impacts of infectious agents extend beyond infected individuals and how, in this way, they are even stronger evolutionary forces than already considered. Here, to evaluate the effects of infection risk on maternal responses, we exposed healthy female Japanese quail to either an immune-challenged (lipopolysaccharide, LPS, treated) mate or to a healthy (control) mate. We first assessed how females responded behaviorally to these treatments. Exposure to an immune-challenged or control male was immediately followed by exposure to a healthy male, to determine whether treatment affected paternity allocation. We predicted that females paired with immune-challenged males would avoid and show aggression towards those males, and that paternity would be skewed towards the healthy male. After mating, we collected eggs over a 5-day period. As an additional control, we collected eggs from immune-challenged females mated to healthy males. We tested eggs for fertilization status, embryo sex ratio, as well as albumen corticosterone, lysozyme activity, and ovotransferrin, and yolk antioxidant capacity. We predicted that immune-challenged females would show the strongest changes in the egg and embryo metrics, and that females exposed to immune-challenged males would show intermediate responses. Contrary to our predictions, we found no avoidance of immune-challenged males and no differences in terms of paternity allocation. Immune-challenged females laid fewer eggs, with an almost bimodal distribution of sex ratio for embryos. In this group, albumen ovotransferrin was the lowest, and yolk antioxidant capacity decreased over time, while it increased in the other treatments. No differences in albumen lysozyme were found. Both females that were immune-challenged and those exposed to immune-challenged males deposited progressively more corticosterone in their eggs over time, a pattern opposed to that shown by females exposed to control males. Our results suggest that egg-laying Japanese quail may be able to respond to infection risk, but that additional or prolonged sickness symptoms may be needed for more extensive maternal responses.
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En las especies con múltiples reproducciones, la inversión en reproducción a menudo disminuye el mantenimiento somático y la supervivencia, generando así un compromiso entre la reproducción actual y las oportunidades para reproducirse en el futuro. En esta pequeña reseña de nuestros estudios mostramos cómo este compromiso modula los conflictos de familia y las estrategias de inversión parental a lo largo de la vida, y puede ser determinado por las presiones de selección durante el desarrollo. Estudiamos cómo las señales sociales, incluidas las sexuales, afectan a las decisiones de inversión parental y pueden ser usadas por todos los miembros de la familia para ajustar su comportamiento, lo que provoca una coevolución social compleja. Nuestros estudios de seguimiento a largo plazo señalan que las estrategias de inversión cambian a lo largo de la vida y están afectadas por el valor de la presente reproducción y por las expectativas futuras. Diversos estudios indican que las trayectorias vitales pueden depender de las presiones selectivas a edades muy tempranas sobre un conjunto de rasgos, y el ambiente social puede ser determinante en su desarrollo. En las últimas décadas, el estudio de los rasgos de comportamiento ha ido cambiado; de examinar cada rasgo de forma independiente a estudiar las relaciones complejas entre rasgos o la coevolución con los rasgos de otros individuos en el entorno social. Quedan muchas preguntas por abordar y para resolverlas se necesitan nuevos estudios y modelos teóricos que recojan la complejidad de factores que afectan a los rasgos de comportamiento.
Age and environment are important determinants of reproductive parameters in long‐lived organisms. These factors may interact to determine breeding responses to environmental change, yet few studies have examined the environmental dependence of aging patterns across the entire lifespan. We do so, using a 20‐year longitudinal dataset of reproductive phenotypes in long‐lived female Nazca boobies (Sula granti), a monogamous seabird breeding in the eastern tropical Pacific. Young and old females may suffer from inexperience and senescence, respectively, and/or practice reproductive restraint. Breeding performance (for breeding participation, breeding date, clutch size, egg volume, and offspring production) was expected to be lower in these age classes, particularly under environmental challenge, in comparison with middle‐aged breeders. Sea surface temperature anomalies (SSTA) represented interannual variation in the El Niño‐Southern Oscillation (ENSO) and were one proxy for environmental quality (a population count of clutch initiations was a second). Although only females lay eggs, both sexes care for eggs and nestlings, and the male partner’s age, alone or in interaction with female age, was evaluated as a predictor of breeding performance. Middle‐aged females performed better than young and old birds for all reproductive traits. Pairing with a young male delayed breeding (particularly for old females) and reduced clutch size, and pairing with an old male reduced offspring production. Challenging environments increased age effects on breeding probability and breeding date across young to middle ages and for offspring production across middle to old ages. However, important exceptions to the predicted patterns for clutch size and fledging success across young to middle ages suggested that trade‐offs between fitness components may complicate patterns of trait expression across the lifespan. Relationships between breeding participation, environment, and individual quality and/or experience in young females may also contribute to unexpected patterns for clutch size and fledging success, traits expressed only in breeders. Finally, independent of age, breeding responses of female Nazca boobies to the ENSO did not follow expectations derived from oceanic forcing of primary productivity. During El Niño‐like conditions, egg‐laying traits (clutch size, breeding date) improved but offspring production declined, while La Niña‐like conditions were “poor” environments throughout the breeding cycle.
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Females may maximize their lifetime reproductive output by adjusting their investment in each breeding event to the perceived likelihood of success. The Blue-footed Booby (Sula nebouxii) is a long-lived seabird with facultative siblicide. We examined whether there is differential resource allocation to eggs with laying order and whether greater egg mass increases hatching probability, chick survival, hatching interval, and mass and size at hatching. We found that the relative investment in first and second eggs decreased as the season advanced: second eggs were slightly (1.5%) heavier than first eggs in early clutches; by contrast, first eggs were 2% heavier than second eggs in late clutches. Accordingly, hatching probability increased with laying date for first eggs and decreased for second eggs. The mass of the egg increased hatching probability, and no effect on chick survival was detected. Laying interval increased after a heavier egg was laid, and heavier eggs produced heavier hatchlings. Hatching intervals were positively related to laying intervals, but egg mass was unrelated to the length of the incubation period and the hatching interval. Our results suggest that egg mass influences embryo survival and that Blue-footed Booby females may adaptively allocate resources to eggs of different laying order according to breeding conditions. Variación del Peso de los Huevos y Secuencia de Postura en un Ave con Reducción Facultativa de la Nidada
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Bird eggs begin to lose weight as soon as they are laid but their volume and linear dimensions do not change during incubation. The volume of an egg can be estimated within 2% from the relationship: Volume = $0.51\cdot LB^{2}$, where L is the length and B is the breadth (maximum diameter). The fresh weight of an egg can be estimated within 2% from the relationship: Weight = $K_{W}\cdot LB^{2}$, where $K_{W}$ is a species-specific constant that can be determined empirically or calculated from published data.
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Understanding the mechanisms mediating age-dependent reproductive effort in wild animals is a major challenge in evolutionary ecology. The acquisition of molecules able to deter somatic damage could potentially improve reproductive performance, especially in physiologically compromised individuals. Carotenoids are antioxidants and immunoenhancers that animals can only obtain through diet. We tested in male blue-footed boobies whether carotenoid supplementation during incubation improves condition and reproductive performance, particularly of older males. Old birds showed lower levels of peroxidative damage than middle-aged males; however, changes of males' antioxidant capacity and peroxidative damage were not affected by carotenoid supplementation irrespective of age. Experimental old males displayed more colourful feet than control old males after 13 days of first carotenoid supplementation. The effect of carotenoids on male reproductive performance was dependent upon age: young males receiving extra-carotenoids produced chicks with smaller growth rates than control young males, whereas old males receiving extra-carotenoids produced chicks with higher growth rates than control old males. Our results highlight that carotenoids influence the relationship between age and reproductive performance and suggest a positive effect of carotenoids on reproduction of old males.
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Selection should favor individuals that adjust breeding effort to the breeding value of current reproduction. In long-lived animals that live in highly variable and unpredictable environments, dynamic sexual traits may provide updated information on the condition of the mate and hence, females may adjust breeding effort accordingly. The blue-footed booby is a socially monogamous long-lived tropical seabird with an extended period of biparental care. Males and females display colorful feet during courtship and experimental evidence suggests that foot color has been favored by mutual mate preferences. Foot color is a dynamic carotenoid-based trait that honestly indicates the nutritional and immunological state of the individual, and is related to paternal quality, and females rapidly adjust their investment in eggs according to changes in the mates' foot coloration. Furthermore, there seems to be a trade-off between female ornamentation and fecundity mediated by carotenoid availability, suggesting that males should not prefer highly ornamented females that invest heavily in coloration incurring fecundity costs.Using long-term data, we found that as individuals age and accumulate the negative effects of breeding effort, foot color deteriorates. Interestingly, after nonbreeding events males display more colorful and attractive feet compared to nonskipping males, suggesting that senescence of sexual signaling might be mitigated by taking sabbatical years. Additionally, increased levels of oxidative stress impaired foot color of senescent males, suggesting that oxidative stress affects senescence of a sexual trait and that sexual ornamentation may be more honest in aging animals. Our results highlight the importance of dynamic traits for continuous pair evaluation and the potential life history consequences of investment on sexual ornamentation.
1. Trade-offs between current and future resource allocation can select for elevated reproductive effort in individuals facing mortality. Males are predicted to benefit from increasing investment in costly sexually selected signals after experiencing an acute life span reduction, although few examples of such facultative terminal investment are known. 2. In the mealworm beetle, Tenebrio molitor, males’ odours become more attractive to females following a life-threatening immune challenge. However, the pheromones involved are unknown, hindering further insight into the proximate mechanisms and ultimate consequences of terminal investment. 3. Using chemical and behavioural analyses, we show that the cuticular hydrocarbons (CHCs) of T. molitor are sexually dimorphic and are used by females to locate and select males. Moreover, both male CHCs and glandular pheromones were affected by experimental immune challenge in a fashion that made them more attractive to females. 4. The results suggest that males terminally invest in both short- and medium-range pheromones when they perceive reduced future survival. Moreover, the constitutive and inducible aspects of male and female CHC production are consistent with sex-specific selection on the signalling and defensive functions of CHCs. The implications of terminal investment for ‘dishonest’ signalling and the efficacy of sexual selection are discussed.
Activating the immune system has associated fitness costs, both immediate costs in the form of reduced current reproduction and long-term costs in the form of reduced life span and future reproduction. This indicates that immune system activation can be an important agent in life history trade-offs. In this review, we evaluate the importance of four currencies generally considered as potential mediators of the costs of immune responses in ecological studies: (1) energetic costs, (2) nutrient costs, (3) autoimmunity and (4) oxidative stress, which may be responsible for these trade-offs. A meta-analysis revealed significant elevation of energy consumption during an immune response; however, the magnitude of this energetic cost was only 5-15%. In a direct comparison using similar immune system activation in tits, energetic savings in terms of lowered feeding rate was seven times higher than energetic costs of mounting an immune response. These results do not support the hypothesis that energy is the key proximate currency mediating the costs of immunity. Nutrient savings from immunosuppression seem to be even less beneficial as this constitutes only a minor part of the daily nutrient turnover in the body. In our view, there are some indications that oxidative stress can be an important currency that could mediate both short-term and long-term costs of immune system activation, although direct evidence is so far limited. The importance of autoimmune responses is at this point hard to evaluate owing to limited empirical studies in wild animals. (c) 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Reversed sexual size dimorphism in avian species (females larger than males) may be an adaptive consequence of different roles of males and females in parental care. We examined the alleged division of labour in two-chick broods of the blue-footed booby, using behavioural observation and frequent weighing of chicks. In the first week of parental care, males and females Fed broods at similar frequencies and provided similar masses of food, but females brooded more than males when broods were 5.10 d old. Subsequently, females provided a greater mass of food and frequency of feeds than males until chicks were at least 35 d old (mass) and 60 d old frequency), while attending the brood for just as much time as males until chicks were at least 35 d old. Males and females did nor differ in the tendency to feed frequency and mass the first-hatched-chick differentially. In nearly all components of parental care examined here. and in other studies, the female's contribution is equal to or greater than the male's. Only in clutch attendance and nest defence does the male contribute more than the Female, bur his small size seems unlikely to enhance performance in these activities. Overall, small size appears potentially to limit male provisioning of the brood, and is unlikely to be an adaptation For division of labour in parental care. This result casts doubt on the relevance of the division-of-labour hypothesis for adult size dimorphism.