Females sing more often and at higher frequencies than males in Australian magpies

https://doi.org/10.1016/j.beproc.2020.104045Get rights and content

Highlights

  • Recent research has revealed that female birdsong is more common than previously thought.

  • In a handful of species, females sing more than males.

  • We tested for sex differences in singing behaviour in Western Australian magpies.

  • Females sang more often than males, with higher minimum and maximum frequencies.

Abstract

Birdsong is a particularly useful model for animal communication studies. However, current knowledge is derived mainly from the study of male song, and is therefore incomplete. Here, we investigated whether singing behaviour differs between sexes in the cooperatively breeding Western Australian magpie (Gymnorhina tibicen dorsalis). This subspecies lives in territorial groups, and in our population there is a female-biased sex ratio, which may lead to a high level of female-female competition for males. Observations of 94 magpies (54 females, 40 males) revealed that females sang more often than males. As bird song is a sexually multidimensional signal, we also studied amplitude and structure of the main territorial high-amplitude song in magpie; the carol. We found that females sing at the same amplitude as males, but that male and female carols exhibit differences in frequency. These results highlight the importance of studying female song and may change our perception regarding the evolution of sex-specific traits, given the primary focus on male singing as a sexually selected trait in the literature to date. The next step is to discover additional species in which females sing more than males in order to improve our currently incomplete understanding of the evolution of bird song.

Introduction

Many species, across a wide range of taxa, use vocalisations for territory acquisition and maintenance. Among taxa, songbirds are the best-known examples of an animal that sings to defend an area for reproduction, foraging, and roosting (Hinde, 1956). Although it has been observed in many tropical bird species that both sexes sing, historically most research on bird song has been conducted in temperate regions (Kroodsma and Miller, 1996). From a northern temperate zone-centred view, it is primarily the male that sings and defends a breeding-season territory (Beecher and Brenowitz, 2005). However, recent worldwide surveys provide evidence that female song is phylogenetically widespread and that females also sing in many temperate-breeding species (Odom et al., 2014; Odom and Benedict, 2018; Riebel et al., 2019). The increase in studies in the last ten years suggesting that females sing more than previously thought indicates that selective pressures driving song elaboration in female passerines have been underestimated (Langmore, 1998; Odom et al., 2014; Riebel et al., 2019).

Female territorial song is associated with social systems in which there is either (a) a high level of female-female competition for access to mates and resources (e.g., territories, nest-sites, offspring care, and dominance rank), (b) where male defence is lacking (i.e., if the male departs, dies or is investing in reproductive activities elsewhere, e.g., fairy wren males and sparrows (Davies, 1992)) or (c) where territories are defended throughout the year (Langmore, 1998; Price, 2009; Robinson, 1949). Previous research suggests that females sing for a similar reason as males (i.e., mate attraction, intrasexual competition and territory defence, Cain and Langmore, 2015; Diniz et al., 2019; Krieg and Getty, 2016) and join their mates in complex duets in order to mate-guard or to cooperatively defend territories (Hall, 2004; Langmore, 1998; Slater and Mann, 2004). During duets, pairs vocalize with temporal coordination to produce a more or less stereotyped acoustic pattern (Farabaugh, 1982; Kovach et al., 2014). For species exhibiting a social system that includes multiple sexually mature adults (i.e., group-living species), all individuals in the group may produce a song together, known as a chorus (Baker, 2004; Golabek et al., 2012; Seddon, 2002). In some species, females sing more than males, but such cases are rarely noted in the literature. This pattern has been found in six species to date: (i) the cocos flycatcher (Nesotriccus ridgwayi) (Kroodsma et al., 1987), (ii) stripe-headed sparrow (Peucaea ruficauda ruficauda) (Illes and Yunes-Jimenez, 2009; Illes, 2015), (iii) streak-backed oriole (Icterus pustulatus) (Price et al., 2008), (iv) New Zealand bellbird (Anthornis melanura) (Brunton and Li, 2006; Brunton et al., 2008), (v) superb fairy-wren (Malurus cyaneus) (Cain and Langmore, 2015), and (vi) Australian magpie (Gymnorhina tibicen) (Brown and Farabaugh, 1991; Roper, 2007).

Bird song is a multifaceted behaviour and it is therefore important to study several traits rather than a single trait to better understand this behaviour (Gil and Gahr, 2002). In addition to singing effort, song amplitude - one of the most important parameters for signal transmission - plays a part in sexual selection (Gil and Gahr, 2002). Indeed, high-amplitude songs are important for territorial competition (Brumm and Todt, 2004; Brumm and Ritschard, 2011), female choice (Ritschard et al., 2010; Searcy, 1996), and as a signal of the singer’s quality or motivation (Kroodsma, 1979; Lampe et al., 2010). However, to our knowledge, previous studies primarily focussed on song amplitude differences between males (see for instance Brumm and Slater, 2006; Brumm, 2009; Brumm and Ritschard, 2011; Derryberry et al., 2017), and no study has yet compared differences between the sexes in this parameter. In species where females sing more frequently than males, females can use songs of different amplitude than males for the purposes of intrasexual competition, similar to the trends observed for males in previous studies (Brumm and Todt, 2004; Brumm and Ritschard, 2011).

The Western Australian magpie (G. t. dorsalis) produces a range of complex vocalisations, maintains stable territories throughout the year and both sexes sing (Brown and Veltman, 1987; Deng et al., 2001). Magpies breed cooperatively and live in groups where most adult females attempt to breed each year (Pike et al., 2019). Magpies produce two main types of territorial vocalisations: warbles (low amplitude melodious song) and carols, the main territorial high-amplitude song (Brown and Farabaugh, 1991; Kaplan, 2004). Carols are specific loud and slurred songs that are used to advertise and defend a territory, and are commonly used in a group chorus (Carrick, 1963, 1972). Magpies often emit these songs from arboreal perches of varying heights (possibly to increase signal transmission), but also occasionally from on the ground (M. Dutour, pers obs). Although the functional aspects of territorial vocalisations in magpies are now well documented (Deng et al., 2001; Suthers et al., 2011; McCarthy et al., 2013), there are few studies that explicitly investigate the effect of extrinsic (i.e., mate presence, group size, temperature and daytime hour) and intrinsic factors (i.e., age, sex and condition) on carolling behaviour (Farabaugh et al., 1992; Roper, 2007). Observations conducted on the Tasmanian (G. t. tyrannica; Roper, 2007) and the black-backed (G. t. tibicen; Brown and Farabaugh, 1991) subspecies of magpies suggest that females sing more often than males. Carol syllables are also sex-specific: carols produced by females are more complex structurally than those of males, in terms of number of notes, changes in frequency and amplitude modulation (Brown and Farabaugh, 1991). However, previous research has suggested that the structure of carols produced by the Western Australian magpie is not sex-specific (Baker, 2009).

Utilising a combination of observational research and audio recordings, we investigated whether singing behaviour (carols and warbles, hereafter songs), and the amplitude and structure of the most common song type given (the carol) differ between sexes in the Western Australian magpie. This subspecies lives in territorial groups in which there is a female-biased sex ratio in our study population, potentially leading to high levels of female-female competition for mates. Females in the population have previously been observed suppressing the reproductive attempts of others via persistent aggressive attacks on the nesting female, and nest destruction (A. Ridley, pers obs). In this context, if songs are given in response to intrasexual competition, similar to that observed in other species (Cain and Langmore, 2015; Krieg and Getty, 2016), we predicted that females in our female-biased population would sing more and produce louder carols than males. Furthermore, in line with previous work conducted in another population of Western Australian magpies (Baker, 2009), we expected that the structure of carols would not differ between sexes.

Section snippets

Study species and site

Twenty-four groups of magpies located near Perth (31°94′S, 115°84′E), Western Australia, were used for this study. Half of these groups have been ringed and habituated since 1993 to human presence, therefore allowing observation and vocal recording at a close distance (Ashton et al., 2018; Mirville et al., 2016). All of the group territories are located in urban parklands, and all individuals are habituated to human presence. Western Australian magpies are highly social, living in groups of

Song production

Both time of day and the sex of singing individual were the strongest predictors of the number of songs given (Table 1). Magpies produce more songs in the morning than the afternoon (Table 1; Fig. 2). The number of songs varied between sex, with females singing significantly more often than males (Table 1; Fig. 2). There was no effect of group size and the within-group sex ratio on the number of songs emitted per individual (Table 1).

Amplitude and acoustic similarity of carols

There was no difference in carol amplitude between the sexes (

Discussion

Using a combination of observational research and acoustic analyses, we investigated whether the singing behaviour and the structure of the carols differ between sexes in the Western Australian magpie. Our results indicate that females sang more often than males. Furthermore, carol amplitude does not differ between sexes. However, we found sexual dissimilarity in carol frequency features, with a significantly lower minimum and maximum frequency in males.

To our knowledge, observations of

Conclusions

In summary, our work has revealed factors that influence singing behaviour in the cooperatively breeding Western Australian magpie. We found that singing behaviour is influenced by both sex and time of day. Females sing more often than males, however, they produce carols at the same amplitude. Male and female carols exhibit some differences in frequency, but have similar duration and number of notes, suggesting that the selection pressures influencing male and female singing behaviour vary. The

Funding

This work was supported by a Fyssen Foundation (France) grant awarded to M.D.

Role of the funding source

The funding source had not involvement in the study design, the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the article for publication.

Compliance with ethical standards

All work was carried out under an ethical licence from The University of Western Australia Animal Ethics Committee (Protocol number: RA/3/100/1656) and involved passive acoustic recording designed to minimize disturbance and stress.

Submission declaration and verification

This study has not been published previously and is not under consideration for publication elsewhere. Its submission is approved by all authors and tacitly by the responsible authorities where the work was carried out. Moreover, if accepted, this research will not be published elsewhere in the same form, in English or in any other language, including electronically without the written consent of the copyright-holder.

Author contributions

M.D. and A.R.R. conceived and designed the study. M.D. wrote the manuscript and carried out data collection. All authors discussed results and commented on the manuscript.

Declaration of Competing Interest

None.

Acknowledgements

We thank Eleanor Russell and Ian Rowley who established this magpie project and allowed us to continue work on their Guildford population. We thank the University of Western Australia for logistical support, and all past and current members of the Western Magpie Research Project, especially Lizzie Speechley and Sarah Walsh.

References (82)

  • N.E. Langmore

    Functions of duet and solo songs of female birds

    T. Ecol. Evol.

    (1998)
  • W.C. Liu

    The effect of neighbours and females on dawn and daytime singing behaviours by male chipping sparrows

    Anim. Behav.

    (2004)
  • M. Ritschard et al.

    Female zebra finches prefer high-amplitude song

    Anim. Behav.

    (2010)
  • L.G. Schmidt et al.

    Plasma levels of luteinizing hormone and androgens in relation to age and breeding status among cooperatively breeding Australian magpies (Gymnorhina tibicen Latham)

    Gen. Comp. Endocr.

    (1991)
  • S.A. Zollinger et al.

    On the relationship between, and measurement of, amplitude and frequency in birdsong

    Ani. Behav.

    (2012)
  • B.J. Ashton et al.

    Cognitive performance is linked to group size and affects fitness in Australian magpies

    Nature

    (2018)
  • M.C. Baker

    Information content in chorus songs of the group‐living australian magpie (Cracticus tibicen dorsalis) in Western Australia

    Ethology

    (2009)
  • M.C. Baker

    The chorus song of cooperatively breeding laughing kookaburras (Coraciiformes, halcyonidae: dacelo novaeguineae): characterization and comparison among groups

    Ethology

    (2004)
  • A.M. Baker et al.

    Population genetic structure of Australian magpies: evidence for regional differences in juvenile dispersal behaviour

    Heredity

    (2000)
  • K.S. Berg et al.

    Phylogenetic and ecological determinants of the neotropical dawn chorus

    P. R. Soc. B-Biol. Sci.

    (2006)
  • L. Benedict

    Occurrence and life history correlates of vocal duetting in North American passerines

    J. Avian Biol.

    (2008)
  • R.I. Bowman

    Adaptive morphology of song dialects in Darwin’s finches

    J. Ornithol.

    (1979)
  • E.D. Brown et al.

    Ethogram of the Australian magpie (Gymnorhina tibicen) in comparison to other Cracticidae and Corvus species

    Ethology

    (1987)
  • E.D. Brown et al.

    Song sharing in a group-living songbird, the australian magpie, Gymnorhina Tibicen. Part III. Sex specificity and individual specificity of vocal parts in communal chorus and duet songs

    Behaviour

    (1991)
  • T.J. Brown et al.

    Why birds sing at dawn: the role of consistent song transmission

    IBIS

    (2003)
  • H. Brumm

    Song amplitude and body size in birds

    Behav. Ecol. Sociobiol.

    (2009)
  • H. Brumm et al.

    Song amplitude affects territorial aggression of male receivers in chaffinches

    Behav. Ecol.

    (2011)
  • A. Bruni et al.

    Dawn chorus start time variation in a temperate bird community: relationships with seasonality, weather, and ambient light

    J. Ornithol.

    (2014)
  • D.H. Brunton et al.

    The song structure and seasonal patterns of vocal behavior of male and female bellbirds (Anthornis melanura)

    J. Ethol.

    (2006)
  • D.H. Brunton et al.

    A test of the dear enemy hypothesis in female New Zealand bellbirds (Anthornis melanura): female neighbors as threats

    Behav. Ecol.

    (2008)
  • R. Carrick

    Ecological significance of territories in the Australian magpie

    Proc. Intern. Ornithol. Congr.

    (1963)
  • R. Carrick

    Population ecology of the Australian black-backed magpie, royal penguin and silver gull

    Population Ecology of Migratory Birds: A Symposium, Wildlife Research Report, 2

    (1972)
  • T. Dabelsteen et al.

    Why do songbirds sing intensively at dawn?

    Acta Ethol.

    (2002)
  • N.B. Davies

    Dunnock Behaviour and Social Evolution

    (1992)
  • A.D. Demko et al.

    Male and female signaling behavior varies seasonally during territorial interactions in a tropical songbird

    Behav. Ecol. Sociobiol.

    (2018)
  • E.P. Derryberry et al.

    Ecological drivers of song evolution in birds: disentangling the effects of habitat and morphology

    Ecol. Evol.

    (2018)
  • E.P. Derryberry et al.

    White-crowned sparrow males show immediate flexibility in song amplitude but not in song minimum frequency in response to changes in noise levels in the field

    Ecol. Evol.

    (2017)
  • P. Diniz et al.

    Duetting correlates with territory quality and reproductive success in a suboscine bird with low extra-pair paternity

    Auk. Ornithol. Adv.

    (2019)
  • E.K. Edwards et al.

    The impact of high temperatures on foraging behaviour and body condition in the Western Australian Magpie Cracticus tibicen dorsalis

    Ostrich

    (2015)
  • S.M. Farabaugh et al.

    Cooperative territorial defense in the Australian Magpie, Gymnorhina tibicen (Passeriformes, Cracticidae), a group‐living songbird

    Ethology

    (1992)
  • S.M. Farabaugh

    The ecological and social significance of duetting

  • Cited by (14)

    • Austral birds offer insightful complementary models in ecology and evolution

      2022, Trends in Ecology and Evolution
      Citation Excerpt :

      For example, female red-winged starlings Onychognathus morio in South Africa sing regularly throughout the breeding season while male song declines [37], whereas in the New Zealand bellbird/korimako Anthornis melanura female singing bouts increase as male song decreases [38]. Female Australian magpies Gymnorhina tibicen also sing more frequently than males [39]. Such findings have led to a re-examination of assumptions about sexual selection and sexual dimorphism in birds [40,41] and show how historic and geographical research biases have led to a neglect of female song [34].

    • A dawn and dusk chorus will emerge if males sing in the absence of their mate

      2023, Proceedings of the Royal Society B: Biological Sciences
    • Multi-level combinatoriality in magpie non-song vocalizations

      2023, Journal of the Royal Society Interface
    View all citing articles on Scopus
    View full text