Elsevier

Animal Behaviour

Volume 172, February 2021, Pages 155-169
Animal Behaviour

Female signal jamming in a socially monogamous brood parasite

https://doi.org/10.1016/j.anbehav.2020.10.011Get rights and content

Highlights

  • Female cowbird chatter calls are time-locked to male song onset during duets.

  • Signal jamming via chatter effectively reduces the potency of male song.

  • Females preferentially chatter to pair-bond males prior to the onset of breeding.

  • Females use response chatters less selectively after breeding begins.

Acoustic signalling is vital to courtship in many animals, yet the role of female vocalizations is understudied. Here, we combine observational and experimental methods to assess the courtship function of the female chatter call in brown-headed cowbirds, Molothrus ater. While the chatter call is likely multifunctional, it is frequently used in social interactions and overlapping duets with males during the breeding season. Based on a combination of focal- and scan-sampling data from large naturalistic aviaries, we did not find support for the hypothesis that the chatter call elicits male attention or encourages continued courtship. However, we did find evidence that the chatter call plays a role in pair bond formation, as females preferentially chattered in response to songs from pair-bond males in the 2 weeks leading up to the median date of first copulation. Females were less selective in male-directed chatter use after copulations began. We also found support for the hypothesis that chatter is used to signal-jam male songs. Frame-by-frame video analysis revealed that the majority of female chatter calls were tightly time-locked to song, occurring less than 500 ms after male vocal onset. To test the effect of signal jamming on male song potency, we designed a laboratory experiment in which male song playbacks were jammed by various recorded stimuli. Natural chatter calls more effectively reduced female copulatory responses to song than high-pass filtered chatter calls, suggesting that the low frequencies in natural chatter (2–4 kHz) are important for interfering with male song and reducing its potency. Our results suggest that sexual conflict is operating in cowbird courtship, with signal jamming serving as a mechanism by which females guard, resist or select their mates. We also discuss ways in which cowbird vocal interactions may function cooperatively to coordinate reproduction or transition females into breeding condition.

Section snippets

Study System

Brown-headed cowbirds are generalist, obligate brood parasites found throughout much of North America. Social monogamy is the predominant mating system both in aviaries and in the wild (Darley, 1968, 1982; Friedmann, 1929; Laskey, 1950; Louder, Hauber, et al., 2019; White et al., 2010; Yokel, 1986a, 1989), although some males maintain multiple pair bonds (Yokel, 1986a, 1986b) and certain ecological or demographic conditions may lead cowbirds to be more promiscuous (Elliott, 1980; Strausberger &

Chatter Use Varies Among Females

Over a period of 38 days during the 2018 breeding season, we collected a median of five 10 min focal observation blocks per female (mean number of blocks = 4.8 ± 0.2; minimum = 3, maximum = 6) from each of the two aviaries. Among the 12 females, we observed a total of 588 chatters, 199 leaves and 40 lunges across 570 min of observation. There was considerable variability in chatter use among females. The highest-chattering female produced 165 chatter calls across five 10 min observation blocks (33.0 ± 8.1 

Discussion

In this study, we aimed to elucidate the function of the female chatter call during cowbird courtship, hypothesizing that it may play a role in (1) attracting or sustaining male attention, (2) forming or maintaining pair bonds or (3) signal-jamming the songs of males. We did not find support for the hypothesis that chatter elicits male attention, as the vast majority of male-associated chatter calls immediately followed rather than preceded male actions (Fig. 2). In addition, chattering did not

Author Contributions

H.L.A. conceived focal hypotheses, collected focal-sampling videos, designed and performed focal-sampling analyses, co-designed and co-implemented playback experiments, analysed playback experiment data, co-designed the figures and wrote the paper. A.P. designed and performed scan-sampling analyses, co-designed and co-implemented playback experiments, and co-designed and created the figures. J.S.G. reviewed focal-sampling videos and playback experiment videos. H.B.D. set up aviaries and

Acknowledgments

We thank Lydia Horton for help with focal video collection, Chad Vigil for help with video annotation, Jacob Hahn for providing high-resolution spectrograms, the members of the Karubian Lab at Tulane University for helpful comments on the manuscript and Dr Emily Farrer for providing feedback on statistical approaches. We also thank the three anonymous referees whose valuable feedback strengthened the paper. This work was supported by grant funding from the Natural Sciences and Engineering

References (116)

  • T.H. Clutton-Brock et al.

    Sexual coercion in animal societies

    Animal Behaviour

    (1995)
  • A.M. Dufty

    Response of brown-headed cowbirds to simulated conspecific intruders

    Animal Behaviour

    (1982)
  • T.M. Freeberg

    Assortative mating in captive cowbirds is predicted by social experience

    Animal Behaviour

    (1996)
  • T.U. Grafe et al.

    Functions of duetting in the tropical boubou, Laniarius aethiopicus: Territorial defence and mutual mate guarding

    Animal Behaviour

    (2004)
  • M.L. Hall et al.

    Temporal coordination signals coalition quality

    Current Biology

    (2007)
  • L. Marshall-Ball et al.

    Multiple functions to duet singing: Hidden conflicts and apparent cooperation

    Animal Behaviour

    (2006)
  • A.L. O'Loghlen et al.

    East and west coast female brown-headed cowbirds agree: Both categories of male song are sexy

    Animal Behaviour

    (2002)
  • G.A. Parker

    Sexual selection and sexual conflict

  • S.I. Rothstein et al.

    The agonistic and sexual functions of vocalizations of male brown-headed cowbirds, Molothrus ater

    Animal Behaviour

    (1988)
  • J.A. Tobias et al.

    Signal jamming mediates sexual conflict in a duetting bird

    Current Biology

    (2009)
  • S.E. Allan et al.

    Lateralization and motor stereotype of song production in the brown-headed cowbird

    Journal of Neurobiology

    (1994)
  • G. Arnqvist et al.

    Sexual conflict and arms races between the sexes: A morphological adaptation for control of mating in a female insect

    Proceedings of the Royal Society of London, Series B: Biological Sciences

    (1995)
  • A.J. Bateman

    Intra-sexual selection in Drosophila

    Heredity

    (1948)
  • D. Bates et al.

    Fitting linear mixed-effects models using lme4

    Journal of Statistical Software

    (2015)
  • L.D. Beletsky

    Vocalizations of female northern orioles

    The Condor: Ornithological Applications

    (1982)
  • L.D. Beletsky

    Intersexual song answering in red-winged blackbirds

    Canadian Journal of Zoology

    (1985)
  • L. Benedict

    Occurrence and life history correlates of vocal duetting in North American

    passerines. Journal of Avian Biology

    (2008)
  • S.M. Birks et al.

    Vocalizations of female red-winged blackbirds inhibit sexual harassment

    Wilson Bulletin

    (1987)
  • P.L.R. Brennan et al.

    The limits of sexual conflict in the narrow sense: Insights from waterfowl biology

    Philosophical Transactions of the Royal Society B

    (2012)
  • P.L.R. Brennan et al.

    Coevolution of male and female genital morphology in waterfowl

    PLoS One

    (2007)
  • K. Burnell et al.

    Variation in the structure of female brown-headed cowbird vocalizations and its relation to vocal function and development

    The Condor: Ornithological Applications

    (1994)
  • C.K. Catchpole et al.

    Bird song: Biological themes and variations

    (2008)
  • B.G. Cooper et al.

    Multimodal signals: Enhancement and constraint of song motor patterns and visual display

    Science

    (2004)
  • A.J. Corcoran et al.

    Tiger moth jams bat sonar

    Science

    (2009)
  • A.J. Corcoran et al.

    Bats jamming bats: Food competition through sonar interference

    Science

    (2014)
  • C.R. Dahlin et al.

    Angry birds need not apply: A perspective on the flexible form and multifunctionality of avian vocal duets

    Ethology

    (2014)
  • M. Daly

    The cost of mating

    The American Naturalist

    (1978)
  • J.A. Darley
    (1968)
  • J.A. Darley

    Territoriality and mating behavior of the male brown-headed cowbird

    The Condor: Ornithological Applications

    (1982)
  • A.M. Dufty

    Movements and activities of radio-tracked brown-headed cowbirds

    The Auk: Ornithological Advances

    (1982)
  • A.M. Dufty

    Singing and the establishment and maintenance of dominance hierarchies in brown-headed cowbirds

    Behavioral Ecology and Sociobiology

    (1986)
  • L.S. Eberhardt

    Oxygen consumption during singing by male Carolina wrens (Thryothorus ludovicianus)

    The Auk: Ornithological Advances

    (1994)
  • P.F. Elliott

    Evolution of promiscuity in the brown-headed cowbird

    The Condor: Ornithological Applications

    (1980)
  • S.M. Farabaugh

    The ecological and social significance of duetting

  • R.C. Fleischer et al.

    Temporal and age-related variation in the laying rate of the parasitic brown-headed cowbird in the eastern Sierra Nevada, California

    Canadian Journal of Zoology

    (1987)
  • T.M. Freeberg et al.

    Social malleability in cowbirds (Molothrus ater artemisiae): Species and mate recognition in the first 2 years of life

    Journal of Comparative Psychology

    (1995)
  • G. Freed-Brown et al.

    Acoustic mate copying: Female cowbirds attend to other females' vocalizations to modify their song preferences. Proceedings of the Royal Society of London

    Series B: Biological Sciences

    (2009)
  • H. Friedmann

    The cowbirds: A study in the biology of social parasitism

    (1929)
  • S. Gavrilets et al.

    The evolution of female mate choice by sexual conflict

    Proceedings of the Royal Society of London, Series B: Biological Sciences

    (2001)
  • A.S. Gersick et al.

    Male cowbirds vary the attractiveness of courtship songs with changes in social context

    Behaviour

    (2018)
  • Cited by (4)

    View full text