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JOURNAL OF AVIAN BIOLOGY 33: 269 – 275, 2002
The natural plasma testosterone profile of male blue tits during
the breeding season and its relation to song output
Katharina Foerster, Angelika Poesel, Hansjo¨rg Kunc and Bart Kempenaers
Foerster, K., Poesel, A., Kunc, H. and Kempenaers, B. 2002. The natural plasmatestosterone profile of male blue tits during the breeding season and its relation tosong output. – J. Avian Biol. 33: 269 – 275.
In male birds, the gonadal hormone testosterone (T) is known to influence territorialand mating behaviour. Plasma levels of T show seasonal fluctuations which vary inrelation to mating system and social instability. First, we determined the natural Tprofile of male blue tits Parus caeruleus during the breeding season. We found thatplasma levels of T increased at the onset of nest building. Thus, the increase incirculating T was not associated with territory establishment, nor with the fertileperiod of the males’ mates. In most individuals, T levels dropped to values close tozero during the period of chick feeding. Second, we investigated the relationshipbetween plasma levels of T and male age, size, and singing behaviour. During themating period, T levels did not differ between 1 yr old and older males and did notcorrelate with body size or condition. However, song output during the dawn chorustended to be positively correlated with T levels. Therefore, if high T levels are costly,song output might be an honest indicator of male quality in blue tits. Finally, weshow that plasma levels of T are significantly higher during the night than during theday. This pattern has also been observed in captive non-passerine birds, but itsfunctional significance remains unknown.
K. Foerster (correspondence), A. Poesel, H. Kunc and B. Kempenaers, Max PlanckResearch Centre for Ornithology, Postfach 1564, D-82305 Starnberg (Seewiesen),Germany. E-mail: k.foerster@erl.ornithol.mpg.de Testosterone (T) plays an important role in driving 1990). In all temperate passerines with paternal care, T male reproductive behaviour in birds. Temporal pat- levels drop rapidly during the incubation phase and are terns in the plasma levels of this sex steroid are trig- low during the period of nestling feeding (e.g. Ball and gered by several factors including photoperiod and Wingfield 1987, Vleck and Brown 1999). T levels may food availability (Wingfield 1983), as well as social show repeated peaks or remain elevated over the entire stimuli (Wingfield et al. 1990). Different T profiles breeding season, when multiple clutches, extra-pair cop- during the breeding season have been related to the ulations, or polygyny are frequent (e.g. Hegner and social systems and the mating strategies of the observed Wingfield 1986, Beletsky et al. 1995, Wada et al. 1999).
bird species (Wingfield et al. 1990, Beletsky et al. 1995, As a consequence of the T-mediated trade-off between Vleck and Brown 1999). Outside the breeding season, sexual behaviour and parental care (Hegner and when competition for nesting sites and copulation part- Wingfield 1987, Beletsky et al. 1995, Raouf et al. 1997), ners is low or absent, plasma levels of T are low high T levels during the late breeding season enable (nonbreeding baseline, sensu Wingfield et al. 1990).
males of these species to acquire additional breeding or When breeding territories are established and when copulation partners, at the cost of reduced paternal mating takes place, T levels rise up to 20-fold to a breeding baseline (e.g. Ball and Wingfield 1987, Vleck T is known to affect also the development of mor- and Brown 1999, Wada et al. 1999). Within the breed- phological, sexually selected traits (e.g. Zuk et al. 1995, ing season, large fluctuations in T levels are observed, Eens et al. 2000, Evans et al. 2000, Peters et al. 2000).
for instance during social challenges (Wingfield et al.
Similarly, the role of T in the expression of behavioural traits involved in sexual selection is well established.
served on 5 March, first eggs were laid on 5 and 6 Males with elevated T levels defend larger territories April, and the last eggs (except for a few replacement (Silverin 1980, Wingfield 1984, Chandler et al. 1994), clutches) between 29 April and 8 May. The period are more aggressive (Beletsky et al. 1990, but see from 5 March to 8 May includes nest building and Romero et al. 1998), and show more elaborate egg laying and was therefore defined as the mating courtship displays (Enstrom et al. 1997, Hill et al.
period. We refer to the periods before and after the 1999) than males with low T levels. Males with high mating period as the territory defence period and the T levels also sing more (e.g. Silverin 1980, Ketterson chick feeding period, respectively.
et al. 1992, Hunt et al. 1997), although some studies Blue tits were captured at night (20:00 – 00:00 hours) have not found this effect (Beletsky et al. 1995, Saino when they slept inside the nestbox and were placed and Møller 1995). Thus, it is evident that elevated T separately in cotton bags. Blood samples (20 – 100 ml) levels as observed in males before and during the from the brachial vein were taken within 30 min of females’ fertile period enable behaviours necessary to capture. During the mating period some males were acquire and defend nest sites and copulation partners.
caught at day in food-baited potter traps. When the However, males vary greatly in their peak level of chicks were 8 – 9 days old, parents were caught inside circulating T, and this might be related to their repro- the nestbox when feeding young. In this case, blood ductive success. Few studies have investigated the ef- samples were taken within 10 min of capture. After fect of this variation on the intensity of sexually centrifugation, plasma was stored at − 70°C until selected traits and sexual behaviour (Erickson 1970, Searcy and Wingfield 1980, Borgia and Wingfield Individuals were colour-banded, sexed and aged (1 yr old or older bird, based on plumage characteristics, In this study, we investigated the natural plasma T Svensson 1992). We measured tarsus length to the levels in a population of blue tits Parus caeruleus nearest 0.1 mm using callipers and body mass to the during the breeding season. This species is mostly so- nearest 0.1 g using a digital balance. We calculated cially monogamous, but polygyny is not uncommon body condition as the residuals of a regression of (Kempenaers 1994). Extra-pair copulations are fre- quent and females choose extra-pair mates that areolder and have longer tarsi than their social partner(Kempenaers et al. 1997). Blue tits are non-migratory Song recording and analysis
and males start singing and defending their territoryas early as January/February, long before nest build- The complete dawn song was recorded once for 28 ing and egg laying. Only during the fertile period of individual males when their females were fertile and the mate, do males show a distinct dawn chorus. A previous study on the same population showed that Windows. For a detailed description of recording song output was related to female fecundity and is methods, song analysis, and song variables see Poesel therefore probably under sexual selection (Poesel et al.
et al. (2001). Here we used two measures of song output: mean strophe length (duration of strophes in The aim of this study was twofold. First, we de- seconds), and mean percentage performance time scribe the temporal changes in natural plasma levels (strophe length divided by the sum of the strophe and of T in male blue tits during the breeding season.
following pause lengths). As mean percentage perfor- Second, we relate plasma levels of T during the pe- mance time declined with recording date (Poesel et al.
riod when T levels are elevated with male characters 2001), we corrected all analyses for recording date.
that are related to their reproductive success, namely Versatility (number of song type switches during the age, size, and song characteristics.
entire dawn chorus multiplied by the number of dif-ferent song types) was used as a measure of songcomplexity. For 10 of the recorded males, the T levelwas measured during their females’ fertile period (song recordings on days 2 to 15, T levels measuredon days Study area and field methods
− 3 to 10, 0 = day of the first egg).
We studied a population of blue tits breeding in nest-boxes in a mixed deciduous woodland at Kolbeter- Hormone analyses
berg in Vienna (48°13%N, 16°20%E), Austria. Duringthe breeding season, nestboxes were checked every An enzyme immunoassay (EIA) was used to assess second day to determine the onset of nest building, the concentration of T in the plasma samples col- laying, hatching, and fledging. In three study seasons lected in 1998. In general, we followed the protocol of (1998 – 2000), the first nest building activity was ob- Palme and Mo¨stl (1993). Five to 20 ml of plasma was diluted 1:10 with double distilled water, extracted with 5 ml diethyl ether and reconstituted in 50 ml assaybuffer. Mean recovery was 84%. The assay sensitivity Temporal changes in plasma levels of T
was 0.06 ng/ml for a plasma sample of 20 ml.
The natural profile of circulating T in blue tit males Plasma samples collected in 1999 and 2000 were during the breeding period changed from low non- analysed in a radio immunoassay (RIA). Seven to 50 ml breeding levels in late winter to high levels at the time of plasma was diluted to 100 ml with assay buffer. We of nest building (Fig. 1a). High T levels were observed used a modification (Fusani et al. 2000) of the RIA from 17 March onwards, two weeks before the first procedure of Wingfield and Farner (1975). The sampleswere reconstituted in 160 ml assay buffer. Mean recov- females in the study area were fertile. Individual males ery was 90% and the sensitivity of the assay was 0.03 showed elevated T levels as early as 27 days before their ng/ml for a plasma sample of 20 ml. The intra-assay social mate became fertile (Fig. 1b). T levels remained variation was 2.8%. All samples were measured in a elevated during egg laying, but dropped when males All measured plasma levels of T fell within the range of the two standard curves (EIA: 0.3 – 80 pg/tube, RIA:0.1 – 200 pg/tube). When analysing hormone levels cor-rected for mean recovery, our conclusions did notchange, and we report uncorrected values.
In 1999 and 2000, some of the resident males in the study area received T-releasing or control implantsduring the mating period. We implanted self-dissolvingpellets with a release time of two months during the lastweek of February and the first week of March (K.
Foerster and B. Kempenaers unpubl.). T levels duringthe mating period did not differ between untreatedmales and males with control implants in these twoseasons (n = 23, x¯ = 1.96 91.48 ng/ml and n=6, x¯=1.61 91.73 ng/ml, resp.; t=0.497, P\0.6). Also, Tlevels of all males (untreated and control-implanted)measured during the mating period did not differamong the three study seasons (each individual usedonly once, Kruskal-Wallis test, H = 2.165, df = 2, P \0.3), or between the two T assay methods (EIA: n = 14,x¯ = 1.74 90.43 ng/ml and RIA: n=15, x¯=1.9590.34ng/ml; Therefore, we pooled all data obtained during themating period.
Data analysis
Statistical analyses follow Sokal and Rohlf (1995) andwere performed using SPSS 10.0 and StatXact 3 forWindows. Plasma levels of T during the mating periodwere normally distributed after log transformation. Weapplied this transformation when testing for correla-tions of T levels with sampling date and time, and with Fig. 1. Natural profile of plasma testosterone levels in resident male characteristics. Untransformed data are presented male blue tits during the breeding season. Data are from 68 as means 9SE, transformed data as back-transformed individuals in three seasons. Circles: T levels measured during means with upper and lower 95% confidence limits. We day, triangles: T levels measured during night. Multiple data applied two-tailed tests and used Bonferroni corrections points are labelled with numbers. (a) T levels in relation tosampling date (1 = 1 Jan). Filled circles: socially polygynous in the case of multiple comparisons.
males, filled triangles: birds not found breeding. The shaded Some males were caught repeatedly over the three area indicates the mating period. (b) T levels in relation to egg years of this study and all data are presented in Fig. 1.
laying of the social mate (0 = day when the first egg was laid).
The shaded area indicates the maximum fertile period of blue For each statistical test we used only one data point per tit females, starting at day − 5 and ending at day 15 (maxi- were feeding nestlings (Fig. 1a). Four polygynous males chick feeding (partial correlation: n = 25, r = 0.44, P = that were sampled during the nestling phase had T levels comparable to those of monogamous males (Fig.
1a).
Samples that were collected at night had higher T Discussion
concentrations than samples collected at day (matingperiod only, night: n = 22, x¯ = 2.31 90.29 and day: This study shows that the profile of plasma levels of T n = 7, x¯ = 0.39 90.10; U=4.0, PB0.001). Also, T lev- in male blue tits during the breeding season follows the els at night were more variable than T levels measured typical pattern of socially monogamous temperate during day (mating period only, Conover test for equal- passerines. The increase in T levels was not associated ity of variances with unequal means, T = 506.0, P = with territory establishment, or with the fertile period 0.01). During the mating period, T levels did not vary of the males’ mates. T levels during the mating period with date or sampling hour (ANCOVA: day/night sam- seem to correlate with song output during the dawn chorus, which is a sexually selected trait (Poesel et al.
test for differences in T levels between the three periods The natural profile of plasma levels of T in male blue of the breeding season, we compared only samples tits showed a single, distinct peak at the time whencompetition for breeding sites and copulation partners obtained at either night or day. At the time of territory is high. T levels increased at the beginning of nest defence in January and February, all samples were building, long before females were fertile. This is similar collected at night, and their T levels were significantly to results from other studies showing that T levels lower than those of samples obtained at night during increase at the onset of nest building (e.g. Silverin et al.
the mating period (territory defence: n = 9, x¯ = 0.11 9 1986, Schoech et al. 1991) or, in migratory species, 0.03 and mating period: n = 19, x¯ = 2.32 90.32; U= when females arrive at the breeding sites (e.g. Silverin 0.0, P B0.001). During the mating period, most birds and Wingfield 1982, Hunt et al. 1997). Blue tit males in were captured at night, while all birds were captured at our study population occupied their territories during day when feeding chicks. However, considering only winter (own obs.). Therefore, most males that later daytime samples, T levels still dropped significantly bred on the study plot had already established a terri- from the mating period to the chick feeding period tory long before the onset of nest building (either by (mating period: n = 7, x¯ = 0.39 90.10 and chick feed- occupying the same area as during the preceding spring ing: n = 42, x¯ = 0.16 90.06; U=57.5, P=0.008).
or by establishing a territory sometime during winter).
However, some 1 yr old males arrived in the study areaas late as March and tried to occupy territories. Aggres- Testosterone and male characteristics
sive male-male interactions were frequent at the timewhen T levels started to rise, but also occurred earlier To correlate male characteristics and T levels, we con- (own obs.). Mate guarding was less intensive during sidered only samples taken at night during the mating early nest building compared to when females were period. Samples taken during the day were too few for fertile (K. Foerster and B. Kempenaers unpubl.) Copu- meaningful analyses. Male T levels did not differ be- lations were observed almost exclusively during the tween 1 yr old males and older individuals (1 yr old: female’s fertile period (own obs.). Thus, high T levels in n = 12, x¯ = 1.92 [CI 1.19, 3.11] and older males: n = 9, blue tit males were less correlated with mate guarding x¯ = 1.76 [CI 1.12, 2.76]; t = 0.29, P \0.7). T levels were than with territorial behaviour, as predicted by the not correlated with male size (tarsus: n = 22, r = 0.17, ‘‘challenge hypothesis’’ (Wingfield et al. 1990). How- P \0.4) or male condition (n=17, r = −0.05, P\ ever, territories are also defended during the period of 0.8). Song output during the dawn chorus measured as mean percentage performance time tended to increase Elevated T levels were observed over a period of 4.5 with T level (partial correlation corrected for recording weeks, which is comparable to the pattern found in date: n = 7, r = 0.86, P = 0.03; significance level after other temperate monogamous species (Wingfield et al.
Bonferroni: P = 0.017). Mean strophe length and song 1990, Vleck and Brown 1999). Birds with prolonged versatility were not significantly related to T level (n = competition over access to extra-pair mates, with multi- 7, r = 0.62, P \0.1 and n=5, r =0.42, P\0.4, re- ple clutches, or polygyny maintain high T levels over a spectively). Mean percentage performance time was long period (Hegner and Wingfield 1986, Vleck and positively related to male body mass and condition in Brown 1999, Wada et al. 1999). In our population the prebreeding period (partial correlation: n = 28, r = extra-pair paternity occurs frequently (59.5% of all 0.51, P = 0.007 and r = 0.51, P = 0.007, respectively; broods in 1998 contained at least one extra-pair young, significance level after Bonferroni: P = 0.0125), and also own unpubl. data). However, females produced only tended to correlate with male body mass later during one clutch (with the exception of a few replacement clutches) and laying was highly synchronous (breeding non-significant results should be interpreted cautiously, synchrony index for 1998 – 2000: 69 – 72% see Kempe- as they might be caused by high individual variation naers 1993). Therefore, the availability of possible ex- tra-pair mates for males was limited to a short time Although blue tit females prefer older and larger interval that overlapped greatly with the fertile phase males as extra-pair partners (Kempenaers et al. 1997), of the social partner. Thus, in this population few we did not find any evidence that these characteristics females were fertile during the chick-feeding period were related to T levels during the mating period.
and males did not face the usual trade-off between However, we found that males with higher T levels mating and parental effort. In other species, T has during this period tended to have a higher song output been shown to play an important role in the regula- at dawn. Furthermore, males with higher song output tion of the behaviours involved in this trade-off (Belet- were in better condition before and during the breed- sky et al. 1995, Raouf et al. 1997). Males with high T ing season. Song is a dynamic behavioural trait that levels during the nestling stage feed nestlings less, or plays an important role in mate choice in passerines not at all (e.g. Silverin 1980, Ketterson et al. 1992, (Andersson 1994). In the blue tit, song output might Schoech et al. 1998, Hunt et al. 1999). In blue tits, be under sexual selection, since males with a higher both monogamous and polygynous males had low lev- song output were paired to females that laid earlier in els of circulating T during the nestling stage, compara- the season (Poesel et al. 2001). Several studies have ble to levels before the mating season (with two shown that individual variation in the avian song con- exceptions, see Fig. 1) and provided about half of the trol system and syringe control is influenced by T (e.g.
food to the nestlings (own unpubl. data).
Luine et al. 1980, Smith et al. 1997). Also, T affects We found that plasma levels of T were higher and the frequency of spontaneous song during the day (e.g.
more variable during the night than during the day.
Ketterson et al. 1992, Hunt et al. 1997, but see Saino Higher T levels during night or a peak at the end of and Møller 1995). In this study we show that within a the dark phase have been reported in domestic ducks period of continuous song (dawn chorus), males with (Balthazart 1976), domestic fowl (Bachman et al. 1987, higher T levels tend to have a higher song output. To Schanbacher et al. 1974), and ring doves (Balthazart et our knowledge only one other study has so far related al. 1981). These studies describe circadian patterns ofT levels in captive birds, but the functional signifi- a song characteristic (other than song rate) to T levels cance of the observed differences is unclear (Balthazart during the breeding season: Galeotti et al. (1997) et al. 1981). To our knowledge, our study provides the found that male barn swallows Hirundo rustica with first data on free-living individuals and on a passerine.
high T levels produced longer rattles than males with Our results may have been influenced by the sampling low T levels. Interestingly, that study also showed that methods; handling time during day was generally a characteristic of the rattle (peak amplitude fre- shorter than during night, when birds were trans- quency) was related to body condition. Similarly, we ported to a shed before bleeding. However, several found a relation between song output and condition in studies have shown that T levels were not influenced significantly by long handling times (Wingfield et al.
It is probably costly for a male to maintain high T 1982, Silverin 1998, Kitaysky et al. 1999).
levels over a long period, as T has been shown to be Some studies indicate that the relative concentration immunosuppressive in birds (Verhulst et al. 1999, Pe- of circulating T during the period when T levels are ters 2000, but see Hasselquist et al. 1999). If high T elevated correlates with the intensity of aggressive and levels are costly and the intensity of a sexually selected sexual behaviour (Searcy and Wingfield 1980, Borgia trait depends on T, then this trait might signal male and Wingfield 1991, Enstrom et al. 1997). However, it quality (Folstad and Karter 1992). Thus, our data is still unclear whether the individual variation in T indicate that song output during the dawn chorus levels during the mating period affects male attractive- might provide an honest signal of male quality.
ness to females (Hill et al. 1999). Few studies haveinvestigated correlations between T levels and male Acknowledgements – We thank Katharina Peer and AgnesTu¨rk for help in the field and Cheryl Bishop and Etie¨nne characteristics in free-living birds. Single measurements Vermeirssen for analysing plasma samples. Erich Mo¨stl (Vet- of T levels may depend strongly on time of day (this erinary University, Vienna) and Tom Van’t Hof (Max Planck study) and on the state of the animal prior to sam- Research Centre for Ornithology, Andechs) generously pro- pling. Social interactions quickly raise plasma levels of vided resources and help in their labs. Raphael-ThomasKlumpp and Alfred Fojt from the Institute of Silviculture, T in some bird species (Wingfield and Wada 1989, Vienna, provided access to their facilities in the study area. We Wingfield et al. 1990, Wikelski et al. 1999). Thus, if thank Virginie Canoine, Leonida Fusani, Tom Van’t Hof, and only one sample is taken per individual, large fluctua- two anonymous referees for helpful comments on the tions over time might mask relations of T levels with manuscript. We are grateful to Hans Winkler from the Kon-rad Lorenz Institute for Comparative Ethology (KLIVV), male characteristics. We were not able to take multiple Vienna, for continuous support during this study. KF was measurements during the mating period. Thus, our References
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(Recei6ed 22 December 2000, re6ised 2 August 2001, accepted 4

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