Abstract
In blue petrels (Halobaena caerulea), females are supposed to be particularly choosy and mate choice can take a couple of years. In these lifelong monogamous seabirds, choosing a good mate is crucial and has a strong influence on their fitness. Due to their nocturnal habits, the absence of sexual dimorphism, and the physical barrier between males calling from their burrow and females flying above the colony, vocal signals seem to be one of the main channels for males to communicate with potential mates. In a previous study, we investigated whether acoustic parameters of male calls carry information about morphological characteristics that might be indicators of males’ qualities. Here, we experimentally test whether these acoustic parameters linked to male characteristics are actually attractive to females. To do so, we played back modified calls of males to females in a colony of blue petrels of the Kerguelen archipelago. We found that flying females were more attracted by high-pitched calls, and by calls broadcasted at a high call rate. Previous studies showed a relationship between pitch and bill depth and length. In filter-feeding birds, such as blue petrels, bill morphology influences feeding efficiency. A high call rate is an indicator of sexual motivation and makes the caller easier to locate by potential mates and predators in the hubbub of the colony. We thus hypothesized that producing frequent high-pitched calls appeared to be preferable for a conspicuous sexual signaling although it may increase predation risks.
Significance statement
Mate selection process is largely unknown in burrowing petrels due to their cryptic life at the colony. Here, we examined the implication of vocal signals in mate choice in the blue petrel Halobaena caerulea. We used an experimental setting based on a two-choice test to show that male calls are sexual signals attracting females. As expected, broadcasting male calls attracted females. Despite the apparent stereotypy of male calls, their acoustic parameters transmit pieces of information that may influence females’ preference. We found that females are more attracted by high call rate and high-pitched calls. This is the first evidence of the implication and influence of vocal signals in mate choice in burrowing petrels.





Similar content being viewed by others
Data Availability
The dataset generated and analyzed during the current study is available in supplementary material.
References
Amorim MCP (2006) Diversity of sound production in fish. Diversity 1:71–105
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Aubin T, Jouventin P (1998) Cocktail-party effect in king penguin colonies. Proc R Soc Lond B 265:1665–1673. https://doi.org/10.1098/rspb.1998.0486
Bakker TCM, Pomiankowski A (1995) The genetic basis of female mate preferences. J Evol Biol 8(2):129–171. https://doi.org/10.1046/j.1420-9101.1995.8020129.x
Ballentine B (2009) The ability to perform physically challenging songs predicts age and size in male swamp sparrows, Melospiza georgiana. Anim Behav 77:973–978. https://doi.org/10.1016/j.anbehav.2008.12.027
Ballentine B, Hyman J, Nowicki S (2004) Vocal performance influences female response to male bird song: an experimental test. Behav Ecol 15:163–168. https://doi.org/10.1093/beheco/arg090
Bates D, Maechler M, Bolker B, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. J Stat Softw 67:1–48
Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science 306:835. https://doi.org/10.1126/science.1103001
Bonadonna F, Sanz-Aguilar A (2012) Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition. Anim Behav 84:509–513. https://doi.org/10.1016/j.anbehav.2012.06.014
Bonadonna F, Spaggiari J, Weimerskirch H (2001) Could osmotaxis explain the ability of blue petrels to return to their burrows at night? J Exp Biol 204:1485–1489
Bonadonna F, Villafane M, Bajzak C, Jouventin P (2004) Recognition of burrow’s olfactory signature in blue petrels, Halobaena caerulea: an efficient discrimination mechanism in the dark. Anim Behav 67:893–898. https://doi.org/10.1016/j.anbehav.2003.08.013
Bradbury JW, Vehrencamp SL (2011) Principles of animal communication. Sinauer Associates, Sunderland
Bretagnolle V (1990) Behavioural affinities of the blue petrel Halobaena caerulea. Ibis 132:102–105. https://doi.org/10.1111/j.1474-919X.1990.tb01020.x
Bretagnolle V (1996) Acoustic communication in a group of nonpasserine birds, the petrels. In: Kroodsma DE, Miller EH (eds) Ecology and Evolution of Acoustic Communication in Birds. Cornell University, New York, pp 160–177
Bried J, Jouventin P (2001) Site and mate choice in seabirds: an evolutionary approach. In: Schreiber EA, Burger J (eds) Biology of Marine Birds. CRC Press, Boca Raton, pp 263–305
Brothers NP (1984) Breeding, distribution and status of burrow-nesting petrels at Macquarie Island. Wildl Res 11:113–131. https://doi.org/10.1071/WR9840113
Brumm H, Zollinger SA (2013) Avian vocal production in noise. In: Brumm H (ed) Animal communication and noise. Springer-Verlag, Heidelberg, pp 187–227
Byers BE, Akresh ME, King DI (2016) Song and male quality in prairie warblers. Ethology 122:660–670. https://doi.org/10.1111/eth.12513
Cardoso GC (2012) Paradoxical calls: the opposite signaling role of sound frequency across bird species. Behav Ecol 23:237–241. https://doi.org/10.1093/beheco/arr200
Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations, 2nd edn. Cambridge University Press, Cambridge
Chastel O, Weimerskirch H, Jouventin P (1995) Body condition and seabird reproductive performance: a study of three petrel species. Ecology 76:2240–2246. https://doi.org/10.2307/1941698
Cherry C (1957) On human communication; a review, a survey, and a criticism. The Technology Press of MIT, Cambridge
Christensen R, Kleindorfer S, Robertson J (2006) Song is a reliable signal of bill morphology in Darwin’s small tree finch Camarhynchus parvulus, and vocal performance predicts male pairing success. J Avian Biol 37:617–624. https://doi.org/10.1111/j.0908-8857.2006.03684.x
Courtiol A, Etienne L, Feron R, Godelle B, Rousset F (2016) The evolution of mutual mate choice under direct benefits. Am Nat 188:521–538. https://doi.org/10.1086/688658
Dooling RJ (1982) Auditory perception in birds. In: Kroodsma D, Miller E (eds) Acoustic communication in birds, vol 1. Academic Press, New York, pp 95–130
Favaro L, Gamba M, Gili C, Pessani D (2017) Acoustic correlates of body size and individual identity in banded penguins. PLoS ONE 12:e0170001. https://doi.org/10.1371/journal.pone.0170001
Galeotti P, Sacchi R, Rosa DP, Fasola M (2005) Female preference for fast-rate, high-pitched calls in Hermann’s tortoises Testudo hermanni. Behav Ecol 16:301–308. https://doi.org/10.1093/beheco/arh165
Gémard C, Aubin T, Bonadonna F (2019) Males’ calls carry information about individual identity and morphological characteristics of the caller in burrowing petrels. J Avian Biol 50:jav.02270. https://doi.org/10.1111/jav.02270
Genevois F, Bretagnolle V (1994) Male blue petrels reveal their body mass when calling. Ethol Ecol Evol 6:377–383. https://doi.org/10.1080/08927014.1994.9522988
Gibson RM (1989) Field playback of male display attracts females in lek breeding sage grouse. Behav Ecol Sociobiol 24:439–443. https://doi.org/10.1007/BF00293273
Halliday T (1983) The study of mate choice. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 3–32
James PC (1985) The vocal behaviour of the Manx shearwater Puffinus puffinus. Z Tierpsychol 67(1–4):269–283. https://doi.org/10.1111/j.1439-0310.1985.tb01394.x
Johnstone RA (1995) Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol Rev 70(1):1–65. https://doi.org/10.1111/j.1469-185X.1995.tb01439.x
Jouventin P, Mougin J-L (1981) Les stratégies adaptatives des oiseaux de mer. Rev Ecol 35:217–249
Jouventin P, Aubin T, Lengagne T (1999) Finding a parent in a king penguin colony: the acoustic system of individual recognition. Anim Behav 57:1175–1183. https://doi.org/10.1163/156853999501595
Klages NTW, Cooper J (1992) Bill morphology and diet of a filter-feeding seabird: the broad-billed prion Pachyptila vittata at South Atlantic Gough Island. J Zool 227:385–396. https://doi.org/10.1111/j.1469-7998.1992.tb04401.x
Klump GM (2000) Sound localization in birds. In: Dooling RJ, Fay RR, Popper AN (eds) Comparative hearing: birds and reptiles. Springer, New York, pp 249–307
Knörnschild M, Blüml S, Steidl P, Eckenweber M, Nagy M (2017) Bat songs as acoustic beacons - male territorial songs attract dispersing females. Sci Rep 7:13918. https://doi.org/10.1038/s41598-017-14434-5
Kriesell HJ, Aubin T, Planas-Bielsa V, Benoiste M, Bonadonna F, Gachot-Neveu H, le Maho Y, Schull Q, Vallas B, Zahn S, le Bohec C (2018) Sex identification in king penguins Aptenodytes patagonicus through morphological and acoustic cues. Ibis 160:755–768. https://doi.org/10.1111/ibi.12577
Leclaire S, Strandh M, Mardon J, Westerdahl H, Bonadonna F (2017) Odour-based discrimination of similarity at the major histocompatibility complex in birds. Proc R Soc B 284:201620466. https://doi.org/10.1098/rspb.2016.2466
Lengagne T, Aubin T, Lauga J, Jouventin P (1999) How do king penguins (Aptenodytes patagonicus) apply the mathematical theory of information to communicate in windy conditions? Proc R Soc Lond B 266:1623–1628. https://doi.org/10.1098/rspb.1999.0824
Marler P, Slabbekoorn H (2004) Nature ’s music. The science of Birdsong. Elsevier, Amsterdam
Marten K, Quine D, Marler P (1977) Sound transmission and its significance for animal vocalization. Behav Ecol Sociobiol 2:291–302. https://doi.org/10.1007/BF00299741
Martín-Vivaldi M, Palomino JJ, Soler M (1998) Song structure in the hoopoe (Upupa epops) - Strophe length reflects male condition. J Ornithol 139:287–296. https://doi.org/10.1007/BF01653339
Martín-Vivaldi M, Palomino JJ, Soler M (1999) Function of song in the hoopoe Upupa epops. Bird Study 46:104–111. https://doi.org/10.1080/00063659909461120
Martín-Vivaldi M, Palomino JJ, Soler M (2000) Attraction of hoopoe Upupa epops females and males by means of song playback in the field: influence of strophe length. J Avian Biol 31:351–359. https://doi.org/10.1034/j.1600-048X.2000.310311.x
McComb KE (1991) Female choice for high roaring rates in red deer, Cervus elaphus. Anim Behav 41:79–88. https://doi.org/10.1016/S0003-3472(05)80504-4
Moncorps S, Chapuis JL, Haubreux D, Bretagnolle V (1998) Diet of the brown skua Catharacta skua lönnbergi on the Kerguelen archipelago: comparisons between techniques and between islands. Polar Biol 19:9–16. https://doi.org/10.1007/s003000050210
Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34. https://doi.org/10.1086/282971
Mougeot F, Bretagnolle V (2000a) Predation risk and moonlight avoidance in nocturnal seabirds. J Avian Biol 31:376–386. https://doi.org/10.1034/j.1600-048X.2000.310314.x
Mougeot F, Bretagnolle V (2000b) Predation as a cost of sexual communication in nocturnal seabirds: an experimental approach using acoustic signals. Anim Behav 60:647–656. https://doi.org/10.1006/anbe.2000.1491
Mougeot F, Genevois F, Bretagnolle V (1998) Predation on burrowing petrels by the brown skua (Catharacta skua lönnbergi) at Mayes Island, Kerguelen. J Zool 244:429–438. https://doi.org/10.1017/S0952836998003136
Mountjoy DJ, Lemon RE (1991) Song as an attractant for male and female European starlings, and the influence of song complexity on their response. Behav Ecol Sociobiol 28:97–100. https://doi.org/10.1007/BF00180986
Nowicki S, Searcy WA (2005) Song and mate choice in birds: how the development of behavior helps us understand function. Auk 122(1):1–14. https://doi.org/10.1642/0004-8038(2005)122[0001:SAMCIB]2.0.CO;2
Park TJ, Dooling RJ (1991) Sound localization in small birds: absolute localization in azimuth. J Comp Psychol 105:125–133. https://doi.org/10.1037/0735-7036.105.2.125
Pennycuick CJ (1982) The flight of petrels and albatrosses (Procellariiformes), observed in South Georgia and its vicinity. Philos Trans R Soc B 300:75–106. https://doi.org/10.1098/rstb.1982.0158
Quillfeldt P, Masello JF, Segelbacher G (2012) Extra-pair paternity in seabirds: a review and case study of thin-billed prions Pachyptila belcheri. J Ornithol 153:367–373. https://doi.org/10.1007/s10336-011-0751-9
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reby D, Charlton BD, Locatelli Y, McComb K (2010) Oestrous red deer hinds prefer male roars with higher fundamental frequencies. Proc R Soc Lond B 277:2747–2753. https://doi.org/10.1098/rspb.2010.0467
Riebel K (2009) Song and female mate choice in zebra finches: A review. Adv Study Behav 40:197–238
Ryan MJ (1980) Female mate choice in a neotropical frog. Science 209:523–525. https://doi.org/10.1126/science.209.4455.523
Salton M, Saraux C, Dann P, Chiaradia A (2015) Carry-over body mass effect from winter to breeding in a resident seabird, the little penguin. R Soc Open Sci 2:140390. https://doi.org/10.1098/rsos.140390
Schreiber EA, Burger J (eds) (2001) Biology of marine birds. CRC Press, Boca Raton
Searcy WA, Andersson M (1986) Sexual selection and the evolution of song. Annu Rev Ecol Syst 17:507–533. https://doi.org/10.1146/annurev.es.17.110186.002451
Searcy WA, Beecher MD (2009) Song as an aggressive signal in songbirds. Anim Behav 78:1281–1292. https://doi.org/10.1016/j.anbehav.2009.08.011
Smith JM (1991) Theories of sexual selection. Trends Ecol Evol 6:146–151. https://doi.org/10.1016/0169-5347(91)90055-3
Specht R (2002) Avisoft-saslab pro: sound analysis and synthesis laboratory. Avisoft Bioacoustics, Berlin
Storey AE (1984) Function of Manx shearwater calls in mate attraction. Behaviour 89:73–89
Walker TJ (1957) Studies on the acoustical behavior and taxonomy of the tree crickets (Orthoptera: Oecanthinae) of the eastern United States. PhD thesis, Ohio State University
Warham J (1990) The petrels: their ecology and breeding systems. Academic Press, London
Warham J (1996) Behaviour and vocalizations of Procellaridae, Hydrobatidae and Pelecoididae. In: The behaviour, population biology and physiology of the petrels. Elsevier, Amsterdam
Weimerskirch H, Chastel O, Ackermann L (1995) Adjustment of parental effort to manipulated foraging ability in a pelagic seabird, the thin-billed prion Pachyptila belcheri. Behav Ecol Sociobiol 36:11–16. https://doi.org/10.1007/BF00175723
Zahavi A (1975) Mate selection — a selection for a handicap. J Theor Biol 53:205–214. https://doi.org/10.1016/0022-5193(75)90111-3
Zahavi A (1977) The cost of honesty. Further remarks on the handicap principle. J Theor Biol 67:603–605. https://doi.org/10.1016/0022-5193(77)90061-3
Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Q Rev Biol 73:415–438. https://doi.org/10.1086/420412
Acknowledgements
We thank Jessica Graham who improved the English of this manuscript, and Guilhem Battistella and Jean-Yves Barnagaud for their precious help on the field. Additionally, we thank two anonymous reviewers for their helpful comments, which improved and clarified the manuscript.
Code availability
Not applicable
Funding
The study was financially supported by the French Polar Institute Paul Emile Victor (IPEV). This work was carried out under the IPEV research program no. 354 ETHOTAAF.
Author information
Authors and Affiliations
Contributions
All authors made substantial contributions to the conception of experiment, analysis and interpretation of data, and critical review of the manuscript. CG, FB, and TA contributed to the study conception and design. CG and FB performed material preparation and data collection. CG and ELR analyzed the data. The first draft of the manuscript was written by CG, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
All experiments were approved by the French Ethical Committee (APAFIS#9496-201707131540776) after favorable recommendation of Comité d’Ethique pour L’Expérimentation Animale Languedoc-Roussillon (CEEA-LR), C2EA no. 36, and by the Ethical Committee of Reserve Naturelle des Terres Australes et Antarctiques Françaises (TAAF). The experiments were made in full conformity with guidelines established by both IPEV and CNRS for the Ethical Treatment of Animals. All experiments comply with the current laws of the country where they were performed.
Consent to participate
This article does not contain any studies involving human participants performed by any of the authors.
Consent for publication
All the authors have approved the submitted version and have agreed both to be personally accountable for their own contributions and to ensure that questions related to the accuracy or integrity of any part of the work, even ones in which the authors were not personally involved, are appropriately investigated and resolved, and the resolution documented in the literature.
Conflict of interest
The authors declare that they have no conflict of interests.
Additional information
Communicated by J. Podos
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 5920 kb)
Rights and permissions
About this article
Cite this article
Gémard, C., Aubin, T., Reboud, E.L. et al. Call rate, fundamental frequency, and syntax determine male-call attractiveness in blue petrels Halobaena caerulea. Behav Ecol Sociobiol 75, 55 (2021). https://doi.org/10.1007/s00265-021-02989-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-021-02989-3


