Ethology

The role of melanin- and carotenoid-based plumage coloration in nest defence in the Great Tit Javier Quesada & Juan Carlos Senar Unidad Asociada CSIC de Ecologı´a Evolutiva y de la Conducta, Museu de Cie`ncies Naturals de Barcelona, Barcelona, Spain

Correspondence Javier Quesada, Laboratorio de Ecologı´a Funcional, CIEco: Centro de Investigaciones en Ecosistemas, Antigua Carretera a Pa´tzcuaro No. 8701 Col. Ex-Hacienda de San Jose´ de La Huerta CP 58190 Morelia, Michoaca´n, Me´xico. E-mail: [email protected]

Received: May 30, 2006 Initial acceptance: July 10, 2006 Final acceptance: February 6, 2007 (L. Sundstro¨m) doi: 10.1111/j.1439-0310.2007.01364.x

Abstract Although plumage coloration is recognized to convey valuable information about the bearer’s parental abilities, few studies have explored the relationship between coloration and nest defence. In this study in Great Tit Parus major, we analysed the relationship between nest defence and melanin- as well as carotenoid-based plumage coloration, after controlling for ecological variables known to influence nest defence. A principal components analysis was applied to classify birds according to how vigorously they defended the nest, and the intensity of nest defence was tested against plumage coloration. Males with a large black tie defended their nests more vigorously, but no such effect was found for yellow breast coloration. This suggests that melanin-based coloration in the Great Tit is associated with aggression, including both dominanceaggression and nest defence, whereas carotenoid-based coloration is not. The challenge in future studies will be to demonstrate whether females use this trait as an ornament to assess male quality and whether they trade off between the different ornaments a male may exhibit.

Introduction Plumage coloration in birds usually arises either from pigment molecules embedded in the feathers or from structural feather properties (Brush 1978). Carotenoids and melanins are the two main pigment molecules responsible for the colourful plumage of a wide variety of bird species. Carotenoids are responsible for red and yellow coloration while melanins are normally responsible for black (eumelanins) and reddish and brown (pheomelanin) colours (Jawor & Breitwisch 2003). Melanin-based ornaments appear to function more commonly in intrasexual competition and they are usually related to dominance status and general aggression (Senar 1999, 2006; Jawor & Breitwisch 2003; Maynard Smith & Harper 2003; but see Griffith et al. 2006), although some relationship to parasite load (Fitze & Richner 2002; Roulin & Dijkstra 640

2003) or body condition (Veiga & Puerta 1996; Roulin & Dijkstra 2003) has also been recognized. Dominant individuals are usually more aggressive, are more involved in contests and are less likely to avoid agonistic encounters (Senar 2006). This could also favour a less evasive behaviour in these individuals towards other species. A case of this interspecific behaviour is the nest defence displayed by parents against a predator. Hence, we could expect that dominant individuals of species which use melaninbased traits in intra-sexual competition could also exert a more vigorous nest defence against predators. To examine this possibility, we investigated whether the size of the melanin-based black tie of the Great Tit Parus major was positively related to a greater nest defence. The Great Tit presents a ventral black tie which works as signal of social status, so that those individuals with a larger black tie are Ethology 113 (2007) 640–647 ª 2007 The Authors Journal compilation ª 2007 Blackwell Verlag, Berlin

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more dominant and aggressive (Ja¨rvi & Bakken 1984; Lemel & Wallin 1993). In addition, Norris (1990b) found that males with a larger black stripe area were more likely to be in the vicinity of their nest and to attend it, considering this as an indirect measure of nest defence. However, although nest attendance (measured by Norris) is a necessary condition for nest defence, to be effective this defence requires active and risky behaviours, so that variables such as distance of approach to the predator or alarm call rate need also to be measured (Radford & Blakey 2000). The aim of our study was therefore to relate the melanin-based black tie of the Great Tit to active nest defence as quantified by Radford & Blakey (2000). The Great Tit also presents a conspicuous yellow coloration on breast and ventral areas which, like the black tie, is also displayed in sexual courtship (Gosler 1993). Individuals with the strongest yellow coloration are in better nutritional and body condition (Dufva & Allander 1995; Ho¨rak et al. 2001; Senar et al. 2003), and provide more food to the nest (I. Ruiz & J. C. Senar, unpub. data). Species simultaneously displaying both melanin- and carotenoidbased plumage coloration have recently been recognized to provide the most robust approach to test for a possible different role of the two colorations (Griffith et al. 2006). This approximation allows the comparison of two traits of plumage colourations in the same conditions and in the same individual. We hence tested for a relationship of nest defence with the carotenoid-based yellow breast as well as with the melanin-based black tie. If the roles of the two colorations differed, we predict that if the size of the black tie was related to nest defence, the colour of the yellow breast would not be. Materials and Methods Great Tits were studied in spring 2002 at Can Cata` field station (Barcelona, NE Iberian Peninsula) (see Figuerola & Senar 2005 for more details) where 171 nest-boxes were distributed. Nest-boxes were visited every 4 d to determine nest building state, laying day, hatching day and brood size. Once we knew the hatching date, nests were only visited on the experimental day to record nest defence rates. To measure nest defence, we focused on males. We used only for analyses the nests in which the female was present (n ¼ 29, first brood nests). Because female Great Tits also defend the nest (Radford & Blakey 2000; Quesada & Senar, pers. obs.) and because parental care by one partner can Ethology 113 (2007) 640–647 ª 2007 The Authors Journal compilation ª 2007 Blackwell Verlag, Berlin

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modify the behaviour of the other partner, we indirectly controlled the effect of the female nest defence by taking its age (i.e. experience) and body condition into account. Measurements of nest defence were initiated when nestlings were 16 d old (nestling period is 18–22 d), first, because males defend the brood more frequently (Regelmann & Eberhard 1986) and more vigorously than females when nestlings are older (Rytko¨nen et al. 1993; Curio & Onnebrink 1995) and second, to standardize for nestling age (Radford & Blakey 2000; Curio 2003). To elicit nest defence by the male, an observer stood approx. 30 cm from the nest; the largest nestling was picked up and induced to utter alarm calls. We used the nestlings from the nest of interest because it has previously been demonstrated that parents defend their own young more vigorously than chicks from another nest (Chaiken 1992). If the male failed to arrive within 2 min, the nestling was exchanged for another. When the male arrived, we measured nest defence variables, also for 2 min. Using chicks for longer periods (e.g. 5 min) could have caused nestlings to tire and to reduce their response (Quesada & Senar, pers. obs.). Furthermore, as body condition may affect the intensity of calls we also measured mean body condition of the chicks. Four of the 29 nestlings needed an additional stimulus to utter alarm calls and this was provoked by gently pinching their rump with the fingertips. We did not observe any anomalous behaviour in stimulated chicks (Quesada & Senar, pers. obs.). As most nestlings began to utter distress calls as soon as they were picked up from the nest, we kept the chick in the dark cupped in the observer’s hands. To standardize calls by nestlings, these were allowed to call for only 5 s each 20 s until the male arrived or while nest defence was measured. For each male, we measured: (1) ‘Latency’ (in seconds): the time elapsed from the chick’s first distress call until the father’s first response call. As we used more than one chick for the same male in some cases (nnest ¼ 4) and we stimulated each chick for 2 min, the latency was computed as: Latency ¼ [No. unsuccessful chicks · (120 s)] + No. seconds elapsed in successful chick; (2) ‘Call rate’: frequency of male alarm calling (Number of calls per minute); and (3) ‘Approach’: closest distance between the male and the observer (Approach). The number of variables quantifying the intensity of nest defence was reduced to one by means of a principal components analysis (PCA) prior to use in the statistical analysis (Rytko¨nen 2002). 641

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Parents were trapped immediately after the nest defence experiment was carried out on day 16 and on subsequent days. We hung an acetate flap on the internal side of the nest entrance so that birds could enter the nesting box by gently pushing the flap, but could not then go out. Once captured, we measured plumage coloration (both melanin- and carotenoidbased colours), body mass and tarsus length, assessed their age (Svensson 1992) and released them. To measure the black tie area, we placed the birds on a surface with mm graph paper as reference and took a digital photo. For each individual, we then measured the size of the melanin-based black breast tie with the program Image Tool 3.0ª (University of Texas, Houston, TX, USA) (Figuerola & Senar 2000). The tie size was calculated from the measurement of a 3 cm wide area beginning 2 cm from the upper border and including the entire width (Fig. 1). This location is most commonly used in other studies on the Great Tit breast tie (Ja¨rvi & Bakken 1984; Norris 1990a; Wilson 1992) but our method measures the true area rather than previous linear measurements used, allowing a higher repeatability (Ri ¼ 0.86 for males, p < 0.005, n ¼ 12, data from Figuerola & Senar 2000). We standardized breast patch size for body size by using the residuals of a regression of tarsus length and area of the black tie, after summing the mean value of population to the residuals. We considered the area of the black tie rather than its colour properties as prospective analyses have shown that in the Great Tit, nest defence is not related to melanin colour variation (Quesada & Senar, unpub. data) and because the ecological significance of this ornament in the Great Tit is related to the area of the tie (Senar 1999 and references therein). To measure yellow chest coloration, we collected 10–12 feathers from a standard spot (Senar et al. 2003; Figuerola & Senar 2005) in the chest of each bird. These were distributed to imitate the body surface (Quesada & Senar 2006) and the mean of three

3 cm 2 cm

Fig. 1: Area used to measure the size of the black tie in the Great Tit.

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measurements of the sample was recorded. This method is very repeatable and comparable to a direct measurement on the plumage of the bird (Quesada & Senar 2006). The colour of the feathers was recorded using spectrophotometer Minolta CM-2600d, which measures from 360 to 700 nm and provides values of lightness, chroma and hue (LCH) using the standard software provided by the instrument. However, the algorithms to calculate LCH variables refer only to the 400–700 nm range and omit the UV region. For this reason, and given that the maximum peak of absorbency of the fourth cone of vision in the UV range in Blue Tit Parus caeruleus is k ¼ 371 nm (Hart et al. 2000), we included Reflectance at 370 nm to take into account UV reflection. We should point out, however, that both visible and UV regions are considerably correlated in the Great Tit (Senar & Quesada 2006). We measured all spectra in reference to a white standard (WS-1, Diffuse Reflectance Standard) (reflectivity over 98%) and in reference to a dark spectrum to avoid external light contamination. We summarized yellow coloration variables in a principal component analysis (PCA) (MacDougall & Montgomerie 2003; Figuerola & Senar 2005). PCA (unrotated solution) conveyed a first Axis (PC1), which explained 49% of variance in carotenoidbased plumage coloration (factor scores: reflectance370nm: 0.88; lightness: 0.92; chroma: 0.47; hue: 0.37). A second axis (PC2) explained 35% of the variance and established a gradient between hue and chroma values (factor scores: intensity370nm: )0.30; lightness: 0.37; chroma: )0.74; hue: 0.78). We then included these two axis (whole variance explained by two axis ¼ 89%) in the analysis. Nest defence rate (as obtained from the PCA) was used as the dependent variable in a backward multiple regression and male plumage colour variables as predictors. In addition to plumage colour variables, we also added different covariate variables to the regression model. These variables are known to influence nest defence. Covariates included were: parent experience (Knight & Temple 1986) (age of the parents, EURING nomenclature), laying date (Montgomerie & Weatherhead 1988), number of nestlings when the experiment was performed (Curio & Onnebrink 1995), and body condition of parents (Hogstad 2005) and nestlings (nest mean). We computed body condition as mass/tarsus length3 (Møller 1989; Perrier et al. 2002). G-Power Program Analysis (Erdfelder et al. 1996) was used when necessary to analyse the power of the tests. Ethology 113 (2007) 640–647 ª 2007 The Authors Journal compilation ª 2007 Blackwell Verlag, Berlin

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Results PC1 from a PCA (unrotated solution) on the nest defence variables was the only component with eigenvalue >1 (variance explained: 62%, n ¼ 29). ‘Call rate’ and ‘Approach’ were the two nest defence variables with the highest weights in PC1, both showing high factor loadings (>0.70) and also high communalities (>0.60) (Table 1). Latency, however, was also significant in the PC1 but it did not show high factor loading or communality (Table 1). We used PC1 as a proxy for the intensity of defence behaviour in the Great Tit. Prior to the main tests we also tested for differences in defence displayed by parental males when nestlings were stimulated and not stimulated to give alarm calls. The difference between the two groups was not significant (oneway anova, F1,27 ¼ 0.06; p ¼ 0.81). The whole model of multiple regression was marginally significant but the power of the test was very high (90%) (Table 2). Our results showed that nest defence was more vigorous when more nestlings were present (Table 2). The yellow breast coloration was not associated with the intensity of nest defence (Table 2) while such an association was significant and positive for the black stripe area once standardized by ecological variables which could affect defence (Table 2). The final regression model was significant and showed similar results (Table 2). Because we were also interested in the effect of particular defence parameters, we analysed the data by analysing each one of these against the remaining set of parameters: ‘Latency’ was not related to any independent variable while ‘Call rate’ was positively related to body condition of male and laying date (Table 3). The area of the black tie and male body condition was significantly and positively related to closest approach (Table 3). Furthermore, instead of collapsing the variables defining carotenoid coloration into a PCA we considered them separately in order to determine whether any particular colour

Table 1: Principal component analysis (PCA) of nest defence variables PC1 factor loadings Latency Call rate Approach Eigenvalue Explained variance

0.66 0.87 )0.81 1.85 0.62

Communalities

R2

0.43 0.76 0.66

0.16 0.41 0.35

Ethology 113 (2007) 640–647 ª 2007 The Authors Journal compilation ª 2007 Blackwell Verlag, Berlin

Table 2: Multiple regression analysis relating nest defence (PC1) to black stripe area and yellow breast coloration (PC1 & 2). Variables that could additionally be related to nest defence have been included in the analyses in order to standardize for their effect Backward multiple regression (n ¼ 29) Whole model (R ¼ 0.73 p ¼ 0.08, Power ¼ 90%) Intercept Laying date Age male Male body condition Age female Female body condition No. of nestlings Nestlings body condition (x) PC1 yellow coloration PC2 yellow coloration Black tie area Final model (step 7) (R ¼ 0.64, p < 0.01) Intercept Male body condition No. of nestlings Black tie area

b

SE

t(18)

p-level

0.26 0.05 0.34 )0.13 0.15 0.38 )0.02

0.21 0.19 0.20 0.17 0.18 0.18 0.18

)1.24 1.22 0.29 1.73 )0.77 0.86 2.11 )0.11

0.23 0.24 0.78 0.10 0.45 0.40 0.05 0.92

0.16 0.24 0.35

0.19 0.18 0.21

0.82 1.31 1.69

0.42 0.21 0.05

t(25)

0.25 0.36 0.51

0.16 0.16 0.16

)2.49 1.54 2.27 3.25

0.02 0.14 0.03 0.003

variable of the yellow breast was related to the nest defence. Results again showed no significant relationship between carotenoid variables and nest defence (Table 4). Discussion Here we have shown that, in the same individual, melanin-based but not carotenoid-based coloration is associated with an active nest defence. Furthermore, a separate model analysis also showed that a larger black stripe area indicated a propensity for a closer approach to a potential predator. ‘Approach’ is possibly the riskier of the variables in nest defence, supporting the role of melanins as potential signals in aggressive contexts. Neither here was yellow coloration related to any of the variables of nest defence. Radford & Blakey (2000) also attempted to relate the size of the black stripe area to nest defence in the Great Tit, but their results were non-significant. However, this probably occurred because they measured breast-stripe size as the width of the tie across the sternum, a measure with a very low repeatability (Ri ¼ 0.08). Our method for measuring the size of the black tie was not a linear measurement as 643

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Table 3: Multiple backward regression model for the relationship of the three variables of nest defence (latency, call rate and approach distance) to black stripe area and yellow breast coloration, analysed separately. Backward multiple regression (n ¼ 29) Latency Whole model (R ¼ 0.69, p ¼ 0.15) Intercept Laying date Age male Male body condition Age female Female body condition Nestlings number Nestlings body condition (x) PC1 yellow coloration PC2 yellow coloration Black tie area Call rate Whole model (R ¼ 0.67, p ¼ 0.23) Intercept Laying date Age male Male body condition Age female Female body condition Nestlings number Nestlings body condition (x) PC1 yellow coloration PC2 yellow coloration Black tie area Final model (step 6) (R ¼ 0.61, p < 0.05) Intercept Laying date Male body condition Nestlings number PC2 yellow coloration Approach Whole model (R ¼ 0.64, p ¼ 0.30) Intercept Laying date Age male Male body condition Age female Female body condition Nestlings number Nestlings body condition (x) PC1 yellow coloration PC2 yellow coloration Black tie area Final model (step 8) (R ¼ 0.55, p < 0.01) Intercept Male body condition Black tie area

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Table 4: Multiple backward regression model of nest defence (PC1) analysed with carotenoid-based coloration parameters considered separately instead of collapsing them in a PCA Backward multiple regression (n ¼ 29)

b

SE

0.11 0.12 0.06 0.24 0.13 0.25 0.22 0.09 0.35 0.19

0.22 0.20 0.21 0.18 0.19 0.19 0.19 0.20 0.19 0.22

0.46 0.17 0.51 )0.25 0.18 0.28 )0.15 0.13 0.34 )0.03

0.23 0.20 0.22 0.19 0.19 0.20 0.19 0.21 0.20 0.23

0.42 0.56 0.33 0.35

0.20 0.20 0.18 0.18

0.21 0.27 )0.32 0.02 0.09 )0.20 )0.10 0.12 0.12 )0.58

0.23 0.21 0.22 0.19 0.20 0.20 0.20 0.22 0.21 0.23

)0.37 )0.47

0.17 0.17

t(18)

b

SE

t(16)

p-level

0.25 0.05 0.36 )0.12 0.14

0.23 0.20 0.22 0.23 0.19

)1.16 1.11 0.27 1.65 )0.53 0.73

0.26 0.28 0.79 0.12 0.61 0.48

0.43 )0.03

0.22 0.20

1.98 )0.14

0.07 0.89

)0.09 0.25 )0.21 0.26 0.36

0.54 0.51 0.32 0.34 0.22

)0.17 0.49 )0.65 0.77 1.64

0.86 0.63 0.53 0.45 0.12

p-level

)0.50 0.50 0.62 0.28 1.34 0.67 1.31 1.16 0.42 1.80 0.89

0.62 0.62 0.54 0.79 0.20 0.51 0.21 0.26 0.68 0.09 0.39

)2.01 2.00 0.85 2.34 )1.34 0.94 1.41 )0.79 0.61 1.68 )0.11 t(24)

0.06 0.06 0.41 0.03 0.20 0.36 0.17 0.44 0.55 0.11 0.91

)2.18 2.17 2.83 1.89 1.94

0.04 0.04 0.01 0.07 0.07

t(18) )0.87 0.88 1.28 )1.43 0.11 0.47 )0.96 )0.50 0.55 0.59 )2.49 t(26)

0.40 0.39 0.22 0.17 0.91 0.65 0.35 0.62 0.59 0.57 0.02

3.34 )2.24 )2.84

0.002 0.03 0.01

Whole model (R ¼ 0.74, p ¼ 0.19) Intercept Laying date Age male Male body condition Age female Female body condition Nestlings number Nestlings body condition (x) Intensity370nm Lightness Chroma Hue Black tie area Final model (step 9) (R ¼ 0.64, p < 0.01) Intercept Male body condition Nestlings number Black tie area

t(25)

0.25 0.36 0.51

0.16 0.16 0.16

)2.49 1.54 2.27 3.25

0.02 0.14 0.03 0.003

Radford & Blakey (2000) performed, but a measure of the whole area by digital pictures. This made our approach a more repeatable method to assess the size of the black tie (Ri ¼ 0.86) (see Figuerola & Senar 2000). We used several secondary variables to control for other factors that could mask the relationship of tie size to defence behaviour. This provides a more realistic scenario to work out the probable meaning of tie size. Unfortunately, our study did not analyse brood sex-ratio which, according to Radford & Blakey (2000), could also influence nest defence. However, we should point out that other study has not confirmed this relationship (Lessells et al. 1998). It has also been suggested that the presence of extrapair chicks may affect the degree of male defence, so that low quality males with extra-pair chicks in their nest defend less vigorously than males with a higher paternity certainty (Lubjuhn et al. 1993; Lubjuhn 1995). However, although this factor has not been taken into account in our analyses, our result of a higher defence in birds with larger ties may not be a collateral effect of extra-pair paternity because the size of the black tie is not related to extra-pair Ethology 113 (2007) 640–647 ª 2007 The Authors Journal compilation ª 2007 Blackwell Verlag, Berlin

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Ethology 113 (2007) 640–647 ª 2007 The Authors Journal compilation ª 2007 Blackwell Verlag, Berlin

3

2 PC1 Nest defence

copulations (Strohbach et al. 1998). Hence, both the size of the black tie and paternity certainty seem to affect nest defence independently. Another factor to consider is that the call rate of the nestlings was not measured, raising the question of whether chick calls could be entirely standardized. However, we allowed them to call for a very short period of time (5 s) so that the variance in call rate would presumably be small. Finally a closer approach by males during nest defence could additionally depend on the availability of perches near the nest, but this was not the case in our study, as our study area is practically fully covered in trees, so that perches for a close approach, including the tree where the nest box was fixed, were always available. As predation is a key determinant of fitness during the reproductive period, effective brood defence will dramatically increase fitness (Redondo 1989). Hence, nest defence is one of the parental abilities which a female could focus on to assess male quality of potential mates. Plumage coloration is generally considered to confer information on the abilities of the bearer (Andersson 1994; Hill & McGraw 2006). Melanin-based black patches have generally been related to fighting ability and dominance (Lemel & Wallin 1993; Senar 1999, 2006) and hormonal titres related to aggression in male–male competitive interactions (Jawor & Breitwisch 2003). As melanin coloration seems to be related to contexts of intraspecific aggressive behaviour, particularly between intrasexual interactions (reviewed by Senar 2006), such coloration would logically also be a good candidate to be related to interspecific aggressive behaviour, for instance, nest defence. Norris (1990b) previously suggested that the size of the black tie of the Great Tit was related to nest defence. However, the variable he used to define defence (presence/absence of the male during the trial) was related to nest attendance rather than to true vigorous nest defence. A study on house sparrows showed how adult males with a larger black tie defended nests more vigorously against predators (Reyer et al. 1998). Our data on Great Tits support this last view, relating a larger black stripe area to more active and vigorous nest defence (Fig. 2) even when other ecological factors were controlled. The fact that we did not find any relationship between the Great Tit yellow breast carotenoid-based coloration and nest defence is not surprising, given that melanin- and carotenoid-based colorations are not correlated traits in the Great Tit (Senar et al. 2003). However, this result, in conjunction with the fact that in this species carotenoids but not melanins

1

0

–1

–2 100

120

140 160 180 200 Black tie area (mm2)

220

240

Fig. 2: Relationship between the black breast stripe area of male Great Tits and nest defence displayed (PC1), measured from PCA on different nest defence variables. A larger PC1 refers to males defending from nearer positions and displaying more alarm calls.

are related to nutritional condition (Senar et al. 2003), supports the view that these plumage coloration traits may be related to different units of information, hence, supporting the Multiple Message Hypothesis (Candolin 2003). Species like the Great Tit, in which both melanin- and carotenoid-based plumage colorations are simultaneously displayed, may be the right model species to experimentally test, in a robust way, whether the roles of melanins and carotenoids differ (Griffith et al. 2006). The challenge in future experimental studies will be to demonstrate whether females of Great Tit use these plumage coloration traits as ornaments to assess male quality and whether they may trade-off between the different individual characteristics of the male. Acknowledgements We thank Judith Mateos, Jose´ Carrillo-Ortiz and Lluı¨sa Arroyo for their help in the field and the laboratory. Carolyn Newey checked the English. We also thank our anonymous referees and Liselotte Sundstro¨m for their helpful comments. The Gil family kindly allowed us to work on their property of Can Cata`. Research Project BOS 2003-09589 to JCS and FPI Grant FP2000-6439 to JQ from the Spanish Research Council, Ministerio de Ciencia y Tecnologı´a funded this work. Literature Cited Andersson, M. 1994: Sexual Selection. Princeton Univ. Press, Princeton, NJ.

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