Male Traits and Female Choice in Java Sparrows: Preference for Large Body Size

Ornithol Sci 10: 73–80 (2011)

SHORT COMMUNICATION Male traits and female choice in Java Sparrows: preference for large body size

Ai HASEGAWA1, #, Masayo SOMA2 and Toshikazu HASEGAWA1

1 Department of Cognitive and Behavioral Science, Graduate School of Arts and Sciences, University of Tokyo, 3–8–1 Komaba, Meguro-ku, Tokyo 153–8902, Japan 2 Department of Biology, Faculty of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, Hokkaido 060–0810, Japan

Abstract Estrildine finches are important model species in experimental studies on ORNITHOLOGICAL female mating preferences, but research has focused on only two species from this SCIENCE family, namely, the Zebra Finch Taeniopygia guttata and the Bengalese Finch Lonchura © The Ornithological Society striata var. domestica, and we know comparatively little about other closely related of Japan 2011 species. Therefore, we investigated sexual dimorphism and female choice in the Java Sparrow Padda oryzivora, which also belongs to the family Estrildidae, to open up the potential for comparative research and to better understand sexual selection in this family. First, we took measurements of eight morphological traits of six male and six female Java Sparrows: natural wing length, maximum wing length, tarsus length, tail length, exposed culmen length, bill width, bill depth and body mass. We quantitatively confirmed that Java Sparrows show sexual dimorphism in bill depth, with males having deeper bills than females. Second, we examined individual variation in male courtship songs by analyzing their acoustic and syntactical structure. After collecting data on male morphological and song-related traits, we conducted two-way choice tests to ask which kinds of male traits predicted which males were preferred by female Java Sparrows. In the choice tests, we put a cage with a female in between two cages each containing one male and recorded the position of the female every 30 seconds by point sampling. We performed a stepwise regression analysis to assess the relationship between the time females spent in front of each male and male morphological and song-related traits. The results indicated that females base their preference upon large body size, which is likely to act as a good indicator of male quality. However, no preference was observed for song-related traits or sexually dimorphic bill depth. Perhaps the sexual dimorphism in bill size is instead the evolutionary outcome of male-male competition.

Key words Bill size, Courtship song, Female choice, Java Sparrows, Sexual dimorphism

Since Darwin (1871) proposed that male morphol- between the sexes, because sexual dimorphism is ogy and behaviour have evolved through female mat- considered to be the outcome of selective pressures ing preferences, many studies have been done to that act differentially on males and females. investigate which male trait is the target of female For the study of female choice, several bird species preference. In the evolutionary context, a preference belonging to the family Estrildidae have long been is defined as any trait that biases the probabilities that used as model species. Regarding the ‘sexual dimor- females mate with different kinds of males (Kirkpatrick phism’ in behaviour, song behaviour of Zebra Finches & Ryan 1991). To study how female preferences Taeniopygia guttata and Bengalese Finches Lonchura work in a certain species, it is essential to discern striata var. domestica has been extensively studied. which trait is sexually dimorphic, that is, different Only male Zebra Finches and Bengalese Finches sing. Their songs consist of discrete song elements (Received 24 August 2010; Accepted 13 February 2011) called ‘notes,’ whose ordering follows a finite-state # Corresponding author, E-mail: [email protected] syntax (Honda & Okanoya 1999). Song features pre-

73 A. HASEGAWA et al. ferred by Estrildine females can be divided into two understand sexual selection in this family. Therefore, trait types: performance-related and elaboration- we aimed to investigate female preference for male related (Nowicki & Searcy 2005; Soma et al. 2006a). sexual traits in the Java Sparrow Padda oryzivora, Features of the former are associated with song pro- which belongs to the family Estrildidae. Java Spar- duction, such as song rate or song duration, whereas rows do not exhibit sexual differences in plumage the latter features represent song complexity, such as (Goodwin 1982; Restall 1996). However, it is reported repertoire size, note type repertoire size, or song lin- that the base of the male’s bill becomes swollen and earity. It has been reported that females of Estrildine redder in breeding condition, whereas the female’s finches show preference for both types of male song does not (Goodwin 1982). This description suggests features (Okanoya 2004a; Okanoya 2004b; Soma et the possible existence of sexual dimorphism in the al. 2006a). Of features related to song production, bill of Java Sparrows, but there is no quantitative evi- song rate seems to play an important role in female dence to support this view. The songs of male Java mate choice. Most studies that have investigated the Sparrows are likely to have evolved through female female preference for song rate in Zebra Finches have mate preference as is the case in Zebra Finches and come to the same conclusion: females preferentially Bengalese Finches, but almost nothing is known choose males that sing more frequently (Houtman about them because of the lack of research. 1992; Collins et al. 1994; De Kogel & Prijs 1996; In this study, we first took measurements of mor- Forstmeier 2004). On the other hand, studies of phological traits, including bill depth, to investigate female preference in Bengalese Finches have focused sexual dimorphism in Java Sparrows quantitatively. on song complexity. It has been reported that female We also collected data of male song-related traits of Bengalese Finches have a preference for more com- this species. Then we conducted a female choice plex songs over simpler ones. For example, when experiment to find out which of these traits contribute they hear conspecific songs of large note type reper- to female mate preference. toire size from a speaker, they show copulation solic- itation displays more often than they do when they MATERIALS AND METHODS hear songs of smaller note type repertoire size (Clayton & Pröve 1989). According to Morisaka et 1) Subjects al. (2008), female Bengalese Finches tend to choose Twelve adult Java Sparrows (six males and six more complex songs in an operant experiment using females) were obtained from local pet suppliers and conspecific songs as stimuli. kept in an aviary at the University of Tokyo. All birds While there are numerous reports on male song had pied wild-like plumage except one white male. behaviour and female choice in estrildid finches, rel- None had experienced breeding. Males were kept atively few studies have focused on female preference individually in small wooden cages (17×34.5×23 cm for male morphological traits in this family, and there high or 14.5×29.5×19 cm high) to prevent aggres- is no clear evidence that any male morphological trait sion between birds, and females were housed together functions as the target of female preference. One of in a metal cage (37×41.5×44 cm high). Males and the few well-studied sexually dimorphic traits in females were visually isolated, but they could hear estrildid finches is the bill colour in Zebra Finches, in each other. The birds had constant access to food, which males have redder bills than females. Research- water and crushed oyster shell. Each bird was marked ers have attempted to demonstrate that female Zebra with individual coloured leg bands, with red excluded Finches preferentially mate with males with a redder to minimize a potential effect on mate preference bill. However, most recent studies have failed to pro- (Burley et al. 1982). All birds were kept under a fixed vide evidence for female preference in bill colour 14:10 hr light:dark cycle, under which it is reported (Collins et al. 1994; Vos 1995; Collins & ten Cate that most Java Sparrows stay in breeding condition 1996; Forstmeier 2004). throughout the year (Kato et al. 1995), at an ambient In contrast with the two Estrildine species, in which temperature of 25±2°C. song behaviour, morphology and female choice have been well investigated, other estrildid finches have 2) Morphological measurements received little attention. However, studying female Before choice tests, eight external morphological choice in multiple Estrildine species will allow us to traits were measured for six males and six females. make interspecies comparisons and thus to better The measurements taken included body mass in

74 Female choice in Java Sparrows grams on an electric balance; natural wing length, level for all males in at least three out of the four tarsus length, exposed culmen length, bill width and acoustic characteristics (data not shown). Therefore, bill depth in millimetres using callipers; and maxi- we concluded that the note type categorization per- mum wing length and tail length in millimetres using formed in this research is reliable. For later analysis, a ruler. The Mann-Whitney U test was used to inves- the number of different note types each male had and tigate whether there is a sexual difference in morphol- the mean values of the duration of each song bout ogy in Java Sparrows. were computed. The syntactical complexity of songs was measured 3) Song recordings and song variables using a linearity index score (Scharff & Nottebohm The songs of six male Java Sparrows were recorded 1991). We assigned a letter to each note type and using a microphone (M-AUDIO NOVA) and a pre- described each song as a string of letters. We then amplifier (M-AUDIO MobilePre USB). Songs were analyzed the string and calculated transition probabil- recorded when males sang spontaneously. During ities from one note type to others to obtain a transition recording, males were visually isolated by cardboard matrix (see Fig. 1). partitions and did not have any visual contact with Scharff and Nottebohm (1991) developed a linear- each other or with females. Therefore, all songs were ity index score to estimate the syntactical complexity undirected. The number of songs obtained per indi- of birdsong. The score is calculated by the following vidual ranged between 12 and 38, with an average of formula: 25. We analyzed the acoustic features of songs using S linearity = the sound analysis software Raven Pro 1.3 (Charif et numberofdifferent notes / song al. 2008). We first made sonograms of each song and catego- numberofdifferent trannsitiontypes song/ rized each note into several distinct note types through In this study, we applied this formula to calculate the visual confirmation. Compared to note type categori- linearity index score not for each song bout, but for zation in Zebra Finches, in which inter-observer reli- each individual, by pooling the notes and transition ability can be quite low (Jones et al. 2001), categori- types of all recorded songs of each male. If a song is zation of Java Sparrows is easier because their notes completely linear, that is, only one note type follows are discrete (as seen in Fig. 1a). For each note type, a certain note (e.g. abcdabcd), the linearity index we computed the average duration, the lowest fre- score equals one. On the other hand, if several pos- quency, the highest frequency and peak frequency. sible note types may follow a certain note, the score We confirmed (by ANOVA followed by Tukey’s post- would be lower than one. Thus, a linearity index score hoc test) that the acoustic characteristics of each note closer to zero indicates a more complex ordering of type differed significantly from each other at the 0.05 song notes.

(a)

(b)

Fig. 1. (a) Sonogram showing an example of a Java Sparrow song. (b) The transition matrix of the song shown in the above sonogram. The transition probability of each pair of notes is given in each cell.

75 A. HASEGAWA et al.

4) Measurements of female preference Table 1. Combination of six males and five females for Female mate preferences were measured according choice tests. to the time females spent in front of a certain male in Female 1 Female 2 Male pairs perch choice tests. Of the six female subjects, one was excluded for the choice tests because of an adverse A B AB CD EF physical condition. We placed two small wooden B C AC BE DF cages, each containing one male on either side of a C D AD BF CE plastic cage (HOEI PQ, 33×54×40 cm) into which one of the five females was introduced (Fig. 2). We D E AE BD CF recorded the behaviour of the birds with a digital E A AF BC DE video camera recorder (SONY DCR-SR100). Five females (A, B, C, D and E) and six males (A, B, C, D, E and F) participated in the choice tests. We each of the six males participated in 5 pairs×2 first made fifteen possible pairs of males and then females=10 sessions, and there were 30 sessions in randomly divided the pairs into five groups, each con- total. No bird was used in more than three sessions taining three pairs. We arbitrarily allotted two females per day. to each male group. In this way, each female was There were three possible positions to be recorded tested for two groups (i.e. six male pairs; Table 1). for the female. If the bird was either on the left perch Birds not participating in the experiment were or even closer to the left side, we recorded the posi- moved to another room so that they would not affect tion as ‘left male.’ If it was either on the right perch the tested birds. The experimenter (AH) stayed in the or even closer to the right side, we recorded it as experiment room to count the number of songs pro- ‘right male,’ and if it was between the left and right duced by males during the choice tests, but was hid- perches, where females could stay on the edge of a den by a shelf more than four metres away from the food- or water cup, we recorded it as in the ‘middle.’ test apparatus. The number of 30-second intervals a female spent in An experimental session consisted of two 30-min- each position was regarded as “female stay time”. We ute trials. In each trial, we recorded the position of also recorded male behaviour (mainly song behav- the tested female every 30 seconds (i.e. 60 times per iour) because we considered it might influence female trial) by point sampling, using recorded video. After behaviour. the first trial, the positions of the male’s cages were exchanged for the second trial. For Females 1 and 2 5) Data analysis (Table 1), the male position order was reversed, that We predicted that females would stay longer in is, if male A was on the left during the first trial of front of the male they preferred than in front of the female A, male B was placed on the left during the less preferred male, and that there would be a sig- first trial for female B. Altogether, each of the five nificant association between the differences in the females participated in 3 pairs×2 groups=6 sessions; time females spent in front of each male and the male

Fig. 2. Schematic view of the test design used for choice tests.

76 Female choice in Java Sparrows traits that influenced female choice behaviour. We aspects of male characteristics. first calculated the difference in the time the female The data of the number of different note types, the stayed between paired males (e.g. when female A was average song duration, and the linearity index scores, tested between males A and B, the value was calcu- were all obtained from undirected songs that were lated by subtracting the time female A remained near recorded before choice tests (see the Song recordings male B from the time spent near male A, divided by and song variables section), though the songs females the sum of the time the female stayed in front of either heard during the tests were directed ones. Directed male to take female activity into account). Taking this songs are more stereotyped than undirected ones in value as the dependent variable, we performed a step- Zebra Finches (Woolley & Doupe 2008), but in both wise regression analysis. As independent variables, Zebra and Bengalese finches, the acoustic structure of we used the differences between six representative the two song types is the same (Clayton 1987; male traits, which were selected as described below Okanoya 1997). Therefore, although we did not make between paired males (e.g. for the pair male A and any recordings of Java Sparrow directed songs, and male B, the values were calculated by subtracting cannot compare their structures with those of undi- male B’s value of a certain trait from that of male A). rected songs, we can assume that directed and undi- Additionally, we performed the same stepwise regres- rected songs in Java Sparrows are quite similar in sion analysis but excluding data from male pairs that their acoustic features as is the case in the two other included the white male, to examine the effect of closely related species and that it would cause no white plumage on female preference. problem if we used the song variable data obtained To avoid multi-colinearity before conducting a from undirected songs for the analysis. stepwise regression analysis, we selected the follow- Additionally, assumptions of distributional normal- ing six male traits in which the difference values ity in the dependent variables were tested using the between paired males were to be obtained for the Shapiro-Wilk test to ensure that the precondition for analysis: maximum wing length, which represents the stepwise regression analyses was met. body size; bill depth, in which significant sexual dimorphism exists; the number of different note types, RESULTS average song duration and linearity index score as representative song-related traits; and total song num- 1) Sexual dimorphism in morphology ber as an index of male activity during the choice Male Java Sparrows were larger than females in all tests. The six traits were selected based on the cor- morphological measurements taken except in tarsus relation coefficients between all measured male traits. length (Table 2). The sexual difference in bill depth There was no significant correlation in any pair of the was statistically significant (U=2, P=0.0087), the above six traits after Bonferroni adjustment (P>0.1). bills of males averaged 11.54±0.38 mm, while those Therefore, it can be said that these traits are indepen- of females averaged 11.01±0.20 mm. However, there dent of each other and that they represent different was no significant difference in other morphological

Table 2. Sexual dimorphism and individual variation in the morphology of Java Sparrows.

mean±SD Range Mann-Whitney U test Traits Male Female Male Female U value P value (N=6) (N=6) (N=6) (N=6) Natural wing length (mm) 68.44±1.36 67.26±1.55 66.19–69.95 65.33–69.98 11 0.31 Maximum wing length (mm) 70.15±1.56 69.09±1.30 68.03–72.30 67.13–71.0 8.5 0.15 Tarsus length (mm) 18.37±0.94 18.49±0.52 16.82–19.28 18.00–19.27 17 0.94 Tail length (mm) 45.76±1.50 43.46±2.91 44.23–47.60 39.90–47.73 7.5 0.11 Exposed culmen (mm) 15.93±0.21 15.53±0.62 15.72–16.17 14.97–16.40 12 0.38 Bill width (mm) 9.34±0.33 9.04±0.37 8.90–9.83 8.68–9.66 8 0.13 Bill depth (mm) 11.54±0.38 11.01±0.20 11.07–12.05 10.64–11.22 2 0.0087 ** Body mass (g) 26.58±1.65 25.09±1.29 24.20–28.47 23.40–27.00 8 0.13

**: P<0.01

77 A. HASEGAWA et al. measurements (P>0.1; Table 2). The results show that while there is a general tendency for male Java Spar- rows to be larger than females, sexual dimorphism in this species was especially prominent in bill depth.

2) Individual differences in male songs The analysis of song related variables of six male subjects revealed that the number of different note types each male sang ranged from 4 to 6, with an average of 5.33±0.82. The average song duration of each male ranged from 6.09 to 10.01 s, and the mean value of six male subjects was 7.85±1.84 s. The mean linearity index score ranged from 0.29 to 0.42, with an average score of 0.35±0.06. Fig. 3. The relationship between the difference in female stay time between paired males divided by the sum of the time 3) Female mate preference the female stayed in front of either male and the difference in maximum wing length between paired males. The data points The assumption of distributional normality in the of male pairs that include the white male are indicated as tri- dependent variables was not rejected by the Shapiro- angles, and those of male pairs that do not include the white Wilk test for both data sets (data set including all male are indicated as crosses. The regression line was calcu- male pairs: N=30, W=0.9587, P=0.29; data set lated using all data points. excluding male pairs with the white male: N=20, W=0.9459, P=0.31). This allowed us to perform Table 3. The results of stepwise regression analysis on the stepwise regression analyses. data set including all male pairs to investigate the different The stepwise regression analysis of the dataset values of which male trait predicted the difference in female including all male pairs (N=30) revealed that the dif- stay time between paired males. ference in female stay time between paired males was Regression associated with the between-male difference in max- Traits SE t value P value coefficient imum wing length (Fig. 3, Table 3). The regression coefficient was positive (0.101) and statistically sig- Maximum wing length 0.101 0.0481 2.10 0.0448 * nificant (P=0.0448). However, the other five repre- (Intercept) 0.290 0.106 2.72 0.0110 * sentative trait variables, namely bill depth, the num- *: P<0.05 ber of different note types, average song duration, linearity index score and total song number sung during choice tests, were not included in the regression DISCUSSION equation as statistically significant explanatory variables. This result indicates that female Java Sparrows The aim of our research was to understand sexual chose to stay close to larger males, but we found no selection in the Java Sparrow, with a focus on female evidence that other male traits influenced female pref- preference for multiple sexual traits. We found that erence. there is sexual dimorphism in bill depth and that The stepwise regression analysis on the data set females prefer larger males with longer wings than excluding male pairs with the white male (N=20) smaller ones. The tendency of females to prefer larger yielded the same tendency. Although no variable males was also found when we excluded the data of remained in the regression equation as an explanatory one white male. Therefore, we assume that our results variable at the P<0.05 level, maximum wing length were not greatly affected by the presence of the white was the most appropriate variable for inclusion in the male in the experimental group. model as we loosened the criterion to P<0.15 (regres- We agree with Goodwin’s (1982) description and sion coefficient=0.112, P=0.108). Moreover, the the many unpublished observations of bird breeders, white male was not especially large or preferred by and have quantitatively confirmed that male Java females compared with other males with wild-like Sparrows have deeper bills than females. However, plumage (Fig. 3). Thus, white plumage had appar- our experimental data did not provide us with evi- ently little influence on female preference. dence that deeper bills in males have evolved through

78 Female choice in Java Sparrows

Table 4. Interspecies comparison of mean note types and mean linearity index scores between three domesticated Estrildine species.

Mean Mean linearity Bird species note types index score Java Sparrow 5.33 0.35 This study Zebra Finch 6 ≈1 Zann 1996 Bengalese Finch 9.25 0.33 Honda & Okanoya 1999 female preference. In the absence of such data, it rule out the possibility that with a greater sample size seems that the sexual dimorphism in bill depth might we might find significant sexual dimorphism in other have evolved through male-male competition. Sev- morphological traits, including maximum wing eral authors have suggested that sexual dimorphism length. in bill size in a number of other bird species is driven Regarding statistical analyses, we have to note that by antagonistic interactions among males (Johnson there are problems pertaining to pseudo-replication 1988; Navarro et al. 2009; Greenberg et al. 2010). and statistical non-independence in our analyses Our own observations indicate that the bill is the body because we repeatedly used a limited number of birds part most often used in aggression between male Java (six males and five females) in the choice tests. Sparrows; deeper bills may favour males in overcom- Although we cannot completely avoid pseudo-repli- ing their competitors. To test whether the sexual cation with the present data sets, we made the com- dimorphism in bill depth is truly the outcome of male- bination patterns of tested females and male pairs as male competition, further empirical study is neces- diverse as possible to minimize the effect of pseudo- sary. replication. In this way, we are able to draw conclu- Large body size, the feature experimentally shown sions about female preference in Java Sparrows with to be preferred by female Java Sparrows, can reflect a certain level of confidence. male quality. Thus far, there have been no reports In the experimental environment in our study, we from the Estrildidae that demonstrates female prefer- succeeded in finding female choice behaviour in Java ence for large body size. However, there is ample Sparrows. This indicates that we could make further evidence that body size is substantially affected by investigations of female preference in Java Sparrows early rearing environment. Offspring body size using various experimental paradigms. Moreover, decreases with increasing brood size, which causes a according to the calculation of linearity index scores highly competitive and stressful environment for the of male courtship songs in our research and previous offspring (Zebra Finch: De Kogel & Prijs 1996; studies, male Java Sparrows’ songs are syntactically Bengalese Finch: Soma et al. 2006b), and this effect more complex than those of Zebra Finches, but less on body size is carried over to the next generation complex than those of Bengalese Finches (Table 4). (Zebra Finch: Naguib & Gil 2005). Therefore, large Though our results did not yield direct evidence of body size is likely to act as an ‘honest signal’ reflect- female preference for complex songs, songs are a ing male quality because it is costly to develop potential target of sexual selection and offer an inter- (Andersson 1994). Preferring large males might thus esting theme for comparative research. The moderate favour females in that they will choose males that song complexity in the Java Sparrow among the three gained enough nutrition when they were nestlings and species mentioned above, the relative ease of note which are well developed. type categorization of courtship songs, and the spe- Generally speaking, the traits preferred by females cies’ experimental testability as noted above, all sug- exhibit sexual dimorphism, while morphological gest that Java Sparrows may represent another good measurements taken in our study showed that there model species for the study of sexual selection in the was no significant sexual difference in the preferred Estrildidae. trait, maximum wing length. We have to note, however, that there was a general tendency for males to be larger than females in body size (except in tarsus ACKNOWLEDGMENTS length), although a statistically significant difference We deeply appreciate Kazuo Okanoya, Yoshimasa Seki and was observed only in bill depth. Therefore, we cannot other biolinguistic laboratory members at Riken for helpful

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