Abstract
Mobbing is a prey antipredator behaviour aimed to reduce the risk of predation. The behaviour may be innate and/or learned. Evaluating this behaviour on a large spatial scale can help to explore the mechanisms behind it. Using a playback experiment, I investigated variation in antipredator behaviour in small passerines in response to vocalisation from a potential predator, Eurasian pygmy owl (Glaucidium passerinum), at 105 sites in 35 localities within and outside the owl’s breeding range. While the birds outside the owl’s breeding range did not respond to the owl’s call, they mobbed at about 60% of the sites within the owl’s breeding range. At sites where the birds did not respond to the owl presentation, alarm calls of forest passerines were broadcasted to them. The birds always mobbed in response to the playback of these alarm calls. These results indicate that the birds’ response to the owl call may be a plastic trait induced by learning, while the response to the alarm calls of birds may be innate, as predation pressure in general can be strong enough to cause directional selection on the prey’s response to the alarm signalling of other birds.



Similar content being viewed by others
Availability of data and materials
The raw data are available as an Online Supplementary Material (Table S1).
References
Åbjörnsson K, Hansson LA, Brönmark C (2004) Responses of prey from habitats with different predator regimes: local adaptation and heritability. Ecology 85:1859–1866
Altmann SA (1956) Avian mobbing behavior and predator recognition. Condor 58:241–253
Andreu J, Barba E (2006) Breeding dispersal of Great Tits Parus major in a homogeneous habitat: effects of sex, age, and mating status. Ardea 94:45–58
Arnaud CM, Suzumura T, Inoue E, Adams MJ, Weiss A, Inoue-Murayama M (2017) Genes, social transmission, but not maternal effects influence responses of wild Japanese macaques (Macaca fuscata) to novel-object and novel-food tests. Primates 58:103–113
Audacity Team (2018) Audacity: free audio editor and recorder [Computer application]. Version 2.4.2. https://audacityteam.org/
Barbaro L, Blache S, Trochard G, Arlaud C, de Lacoste N, Kayser Y (2016) Hierarchical habitat selection by Eurasian pygmy owls Glaucidium passerinum in old-growth forests of the southern French Prealps. J Ornithol 157:333–342
Baroni D, Korpimäki E, Selonen V, Laaksonen T (2020) Tree cavity abundance and beyond: nesting and food storing sites of the pygmy owl in managed boreal forests. For Ecol Manag. https://doi.org/10.1016/j.foreco.2019.117818
Bartoń K (2019) MuMIn: multi-model inference. R package version 1.43.6. https://CRAN.R-project.org/package=MuMIn
BirdLife International (2022) Species factsheet: Glaucidium passerinum. http://www.birdlife.org
Bize P, Diaz C, Lindström J (2012) Experimental evidence that adult antipredator behaviour is heritable and not influenced by behavioural copying in a wild bird. Proc R Soc Lond B Biol Sci 279:1380–1388
Blanquart F, Gandon S, Nuismer SL (2012) The effects of migration and drift on local adaptation to a heterogeneous environment. J Evol Biol 25:1351–1363
Blondel J, Thomas DW, Charmantier A, Perret P, Bourgault P, Lambrechts MM (2006) A thirty-year study of phenotypic and genetic variation of blue tits in Mediterranean habitat mosaics. Bioscience 56:661–673
Broughton RK, Hill RA, Bellamy PE, Hinsley SA (2010) Dispersal, ranging and settling behaviour of Marsh Tits Poecile palustris in a fragmented landscape in lowland England. Bird Study 57:458–472
Carlson NV, Healy SD, Templeton CN (2020) Wild fledgling tits do not mob in response to conspecific or heterospecific mobbing calls. Ibis 162:1024–1032
Cepák J, Klvaňa P, Škopek J, Schröpfer L, Jelínek M, Hořák D, Formánek J, Zárybnický J (eds) (2008) Atlas migrace ptáků České a Slovenské republiky. Czech and Slovak Republic bird migration atlas, Aventinum, Praha
Černecký J, Lešo P, Ridzoň J, Krištín A, Karaska D, Darolová A, Fulín M, Chavko J, Bohuš M, Krajniak D, Ďuricová V, Lešová A, Čuláková J, Saxa A, Durkošová J, Andráš P (2020) Stav ochrany vtáctva na Slovensku v rokoch 2013–2018. Štátna ochrana prírody Slovenskej republiky, Banská Bystrica
Coslovsky M, Richner H (2011) Predation risk affects offspring growth via maternal effects. Funct Ecol 25:878–888
Curio E (1978) The adaptive significance of avian mobbing. I. Teleonomic hypotheses and predictions. Z Tierpsychol. https://doi.org/10.1111/j.1439-0310.1978.tb00254.x
da Cunha FCR, Fontenelle JCR, Griesser M (2017) Predation risk drives the expression of mobbing across bird species. Behav Ecol 28:1517–1523
Dingemanse NJ, Both C, Van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond B Biol Sci 270:741–747
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, García Marquéz JR, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46
Dutour M (2022) Season does not influence the response of great tits (Parus major) to allopatric mobbing calls. J Ethol 40:233–236
Dutour M, Lena JP, Lengagne T (2016) Mobbing behaviour varies according to predator dangerousness and occurrence. Anim Behav 119:119–124
Dutour M, Léna JP, Lengagne T (2017a) Mobbing calls: a signal transcending species boundaries. Anim Behav 131:3–11
Dutour M, Lena JP, Lengagne T (2017b) Mobbing behaviour in a passerine community increases with prevalence in predator diet. Ibis 159:324–330
Ekman J (1989) Ecology of non-breeding social systems of Parus. Wilson Bull 101:26–288
Gelman A, Jakulin A, Pittau MG, Su YS (2008) A weakly informative default prior distribution for logistic and other regression models. Ann Appl Stat 2:1360–1383
Gelman A, Su YS (2022) arm: data analysis using regression and multilevel/hierarchical models. R package version 1.13-1. https://CRAN.R-project.org/package=arm
Göth A (2001) Innate predator-recognition in Australian brush turkey (Alectura lathami, Megapodiidae) hatchlings. Behaviour 138:117–136
Griffin AS (2004) Social learning about predators: a review and prospectus. Anim Learn Behav 32:131–140
Gruen B, Leisch F (2008) FlexMix Version 2: finite mixtures with concomitant variables and varying and constant parameters. J Stat Softw 28:1–35
Hartley PHT (1950) An experimental analysis of interspecific recognition. Symp Soc Exp Biol J 4:313–336
Hogstad O (2015) Social behaviour in the non-breeding season in great tits Parus major and willow tits Poecile montanus: differences in juvenile birds’ route to territorial ownership, and pair-bond stability and mate protection in adults. Ornis Norveg 38:1–8
Kalb N, Randler C (2019) Behavioral responses to conspecific mobbing calls are predator-specific in great tits (Parus major). Ecol Evol 9:9207–9213
Kassambara A (2019) ggpubr: 'ggplot2' based publication ready plots. R package version 0.2.1. https://cran.r-project.org/package=ggpubr
Keen SC, Cole EF, Sheehan MJ, Sheldon BC (2020) Social learning of acoustic anti-predator cues occurs between wild bird species. ProcR Soc B. https://doi.org/10.1098/rspb.2019.2513
Kobayashi T (1994) The biological function of snake mobbing by Siberian chipmunks: I. Does it function as a signal to other conspecifics? J Ethol 12:89–95
Krams I, Krama T, Igaune K, Mänd R (2007) Long-lasting mobbing of the pied flycatcher increases the risk of nest predation. Behav Ecol 18:1082–1084
Krištín A, Kaňuch P (2017) Stay or go? Strong winter feeding site fidelity in small woodland passerines revealed by a homing experiment. J Ornithol 158:53–61
Li H, Wen J (2022) Factors influencing the duration of death feigning in Eucryptorrhynchus scrobiculatus and E. brandti (Coleoptera: Curculionidae). J Ethol 40:61–69
Lima SL (2009) Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation. Biol Rev 84:485–513
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Magrath RD, Haff TM, Fallow PM, Radford AN (2015a) Eavesdropping on heterospecific alarm calls: from mechanisms to consequences. Biol Rev 90:560–586
Magrath RD, Haff TM, McLachlan JR, Igic B (2015b) Wild birds learn to eavesdrop on heterospecific alarm calls. Curr Biol 25:2047–2050
Mansournia MA, Geroldinger A, Greenland S, Heinze G (2018) Separation in logistic regression: causes, consequences, and control. Am J Epidemiol 187:864–870
Matechou E, Cheng SC, Kidd LR, Garroway CJ (2015) Reproductive consequences of the timing of seasonal movements in a nonmigratory wild bird population. Ecology 96:1641–1649
Meyer D, Zeileis A, Hornik K (2022) vcd: Visualizing categorical data. R package version 1.4-10. https://cran.r-project.org/web/packages/vcd/
Morand-Ferron J, Quinn JL (2011) Larger groups of passerines are more efficient problem solvers in the wild. Proc Nat Acad Sci 108:15898–15903
Moudrý V, Komárek J, Šímová P (2017) Which breeding bird categories should we use in models of species distribution? Ecol Indic 74:526–529
Murali G (2018) Now you see me, now you don’t: dynamic flash coloration as an antipredator strategy in motion. Anim Behav 142:207–220
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens PMH, Szoecs E, Wagner H (2019) vegan: Community ecology package. R package version 2.5-5. https://cran.r-project.org/package=vegan
Pačenovský S, Šotnár K (2010) Notes on the reproduction, breeding biology and ethology of the Eurasian pygmy owl (Glaucidium passerinum) in Slovakia. Slovak Rapt J 4:49–81
Pačenovský S (2002) Kuvičok vrabčí/Kuvik vrabčí (Glaucidiuum passerinum). In: Danko Š, Darolová A, Krištín A (eds) Rozšírenie vtákov na Slovensku. Birds distribution in Slovakia. Veda, Bratislava, pp 364–367
Pakanen VM, Karvonen J, Mäkelä J, Hietaniemi JP, Jaakkonen T, Kaisanlahti E, Kauppinen M, Koivula K, Luukkonen A, Rytkönen S, Timonen S, Tolvanen J, Vatka E, Orell M (2018) Cold weather increases winter site fidelity in a group-living passerine. J Ornithol 159:211–219
Pitman RL, Deecke VB, Gabriele CM, Srinivasan M, Black N, Denkinger J, Durban JW, MathewsEA MDR, Neilson JL, Schulman-Janiger A, Shearwater D, Stap P, Ternullo R (2017) Humpback whales interfering when mammal-eating killer whales attack other species: Mobbing behavior and interspecific altruism? Mar Mammal Sci 33:7–58
Prokop P, Trnka A (2011) Why do grebes cover their nests? Laboratory and field tests of two alternative hypotheses. J Ethol 29:17–22
R Development Core Team (2020) A language and environment for statistical computing. https://www.R-project.org/
Randler C (2012) A possible phylogenetically conserved urgency response of great tits (Parus major) towards allopatric mobbing calls. Behav Ecol Sociobiol 66:675–681
RStudio Team (2019) RStudio: integrated development for R. Version 1.2.1335. http://www.rstudio.com
Sandoval L, Wilson DR (2012) Local predation pressure predicts the strength of mobbing responses in tropical birds. Curr Zool 58:781–790
Sandoval L, Wilson DR (2022) Neotropical birds respond innately to unfamiliar acoustic signals. Am Nat 200:419–434
Scheurer JA, Berejikian BA, Thrower FP, Ammann ER, Flagg TA (2007) Innate predator recognition and fright response in related populations of Oncorhynchus mykiss under different predation pressure. J Fish Biol 70:1057–1069
Schloerke DC, Larmarange J, Briatte F, Marbach M, Thoen E, Elberg A, Crowley J (2020) GGally: Extension to 'ggplot2'. R package version 2.0.0. https://cran.r-project.org/package=GGally
Ševčík R, Riegert J, Šťastný K, Zárybnický J, Zárybnická M (2021) The effect of environmental variables on owl distribution in Central Europe: a case study from the Czech Republic. Ecol Inform. https://doi.org/10.1016/j.ecoinf.2021.101375
Shurulinkov P, Ralev A, Daskalova G, Chakarov N (2007) Distribution, numbers and habitat of Pigmy Owl Glaucidium passerinum in Rhodopes Mts (S Bulgaria). Acrocephalus 28:159–163
Silk MJ, Croft DP, Tregenza T, Bearhop S (2014) The importance of fission–fusion social group dynamics in birds. Ibis 156:701–715
Slowikowski K (2019) ggrepel: automatically position non-overlapping text labels with 'ggplot2'. R package version 0.8.1. https://cran.r-project.org/package=ggrepel
Šotnár K, Pačenovský S, Obuch J (2015) On the food of the Eurasian pygmy owl (Glaucidium passerinum) in Slovakia. Slovak Rapt J 9:115–126
Šotnár K, Obuch J, Pačenovský S, Jarčuška B (2020) Spatial distribution of four sympatric owl species in Carpathian montane forests. Rapt J 14:1–13
Storm JJ, Lima SL (2010) Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. Am Nat 175:382–390
Stratmann A, Taborsky B (2014) Antipredator defences of young are independently determined by genetic inheritance, maternal effects and own early experience in mouthbrooding cichlids. Funct Ecol 28:944–953
Strøm H, Sonerud G (2001) Home range and habitat selection in the pygmy owl Glaucidium passerinum. Ornis Fennica 78:145–158
Sultan SE, Spencer HG (2002) Metapopulation structure favors plasticity over local adaptation. Am Nat 160:271–283
Szymkowiak J (2021) Wood warblers learn to recognize mobbing calls of an unfamiliar species from heterospecific tutors. Anim Behav 171:3–11
Templeton CN, Zollinger SA, Brumm H (2016) Traffic noise drowns out great tit alarm calls. Curr Biol 26:R1173–R1174
Tilgar V, Moks K (2015) Increased risk of predation increases mobbing intensity in tropical birds of French Guiana. J Trop Ecol 31:243–250
Valcu M, Kempenaers B (2008) Causes and consequences of breeding dispersal and divorce in a blue tit, Cyanistes caeruleus, population. Anim Behav 75:1949–1963
Veen T, Richardson DS, Blaakmeer K, Komdeur J (2000) Experimental evidence for innate predator recognition in the Seychelles warbler. Proc Biol Sci 267:2253–2258
Verhulst S, Perrins CM, Riddington R (1997) Natal dispersal of great tits in a patchy environment. Ecology 78:864–872
Wesołowski T (2015) Dispersal in an extensive continuous forest habitat: Marsh tit Poecile palustris in the Białowieża National Park. J Ornithol 156:349–361
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Wickham H, Romain F, Henry L, Müller K (2019) dplyr: a grammar of data manipulation. R package version 0.8.1. https://cran.r-project.org/package=dplyr
Wickham H (2017) tidyverse: easily install and load the 'tidyverse'. R package version 1.2.1. https://cran.r-project.org/package=tidyverse
Wiebe KL (2004) Innate and learned components of defence by flickers against a novel nest competitor, the European starling. Ethology 110:779–791
Acknowledgements
I am thankful to the two anonymous reviewers for their comments to the first version of this manuscript.
Funding
The present study was partially supported by the Scientific Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic and Slovak Academy of Sciences (VEGA, project No. 2/0076/19).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no conflict of interest.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
10164_2023_781_MOESM1_ESM.txt
Supplementary file2 Table S1. Data matrix. Header: locality_abbrev = abbreviation of locality name; site_No = site number; latitude; longitude; elevation (m a.s.l.); forest_age = forest stand age (years); coniferous = proportion of coniferous trees (%); breeding_range = site location in relation to breeding range of pygmy owl ( within/outside breeding range); response_site = response of small passerine birds to broadcasted the Eurasian pygmy owl call at the site (mobbing/no response); response_locality = response of small passerine birds to the Eurasian pygmy owl call in the locality, i.e. at three sites (mobbing/no response/mixed); ParMajΓÇôCarCar = the abbreviations of species are composed of the first three letters of the scientific genus and species name. Species list: AegCau = Aegithalos caudatus, CarCar = Carduelis carduelis, CerBra = Certhia brachydactyla, CerFam = Certhia familiaris, CyaCae = Cyanystes caeruleus, LopCri = Lophophanes cristatus, ParMaj = Parus major, PerAte = Periparus ater, PoeMon = Poecile montanus, PoePal = Poecile palustris, RegReg = Regulus regulus, SitEur = Sitta europaea (TXT 10 KB)
About this article
Cite this article
Jarčuška, B. Large-scale spatial pattern of bird responses to a potential predator suggests that predator-specific mobbing is a plastic trait. J Ethol 41, 153–162 (2023). https://doi.org/10.1007/s10164-023-00781-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-023-00781-6