Abstract
Breeding habitat choice based on the attraction to other species can provide valuable social information and protection benefits. In birds, species with overlapping resources can be a cue of good quality habitats; species with shared predators and/or brood parasites can increase joint vigilance or cooperative mobbing, while raptors may provide a protective umbrella against these threats. We tested whether the migratory common redstart (Phoenicurus phoenicurus) is attracted to breed near active nests of the great tit (Parus major), a keystone-information source for migrant passerine birds, or a top predator, the northern goshawk (Accipiter gentilis). This system is unique to test these questions because the redstart is a regular host for the common cuckoo (Cuculus canorus). Therefore, we also evaluated other possible benefits coming from the heterospecific attraction, especially in terms of reducing brood parasitism risk. We monitored redstart occupancy rates, onset of breeding, reproductive investment, and followed nest outcomes in terms of brood parasitism, nest predation risk and overall reproductive success. Redstarts avoided breeding near goshawks, but showed neither attraction nor avoidance to breed next to great tits. Both neighbours neither reduced brood parasitism risk nor affected overall nesting success in redstarts. Redstarts may not use heterospecific attraction for settlement decisions, as associations with other species can only exist when some benefits are gained. Thus, environmental cues may be more important than social information for redstarts when breeding habitat choice. Other front-line defence strategies may have a better impact reducing breeding negative interactions, such brood parasitism.
Similar content being viewed by others
Availability of data and material
The data were deposited in Zibahub. https://doi.org/10.25375/uct.19099868.v1
Code availability
Not applicable.
References
Ahola MP, Laaksonen T, Eeva T, Lehikoinen E (2007) Climate change can alter competitive relationships between resident and migratory birds. J Anim Ecol 76:1045–1052. https://doi.org/10.1111/j.1365-2656.2007.01294.x
Avilés JM, Rutila J, Møller AP (2005) Should the redstart Phoenicurus phoenicurus accept or reject cuckoo Cuculus canorus eggs? Behav Ecol Sociobiol 58:608–617. https://doi.org/10.1007/s00265-005-0941-7
Banks B, Beebee TJC (1987) Factors influencing breeding site choice by the pioneering amphibian Bufo calamita. Ecography (cop) 10:14–21. https://doi.org/10.1111/j.1600-0587.1987.tb00733.x
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 Manage. https://doi.org/10.1016/j.foreco.2019.117818
Blanco G, Tella JL (1997) Protective association and breeding advantages of choughs nesting in lesser kestrel colonies. Anim Behav 54:335–342. https://doi.org/10.1006/anbe.1996.0465
Boualit L, Pichenot J, Besnard A et al (2019) Environmentally mediated reproductive success predicts breeding dispersal decisions in an early successional amphibian. Anim Behav 149:107–120. https://doi.org/10.1016/j.anbehav.2019.01.008
Brown M, Lawes MJ (2007) Colony size and nest density predict the likelihood of parasitism in the colonial Southern Red Bishop Euplectes orix - Diderick Cuckoo Chrysococcyx caprius system. Ibis 149:321–327. https://doi.org/10.1111/j.1474-919X.2006.00633.x
Burgas D, Ovaskainen O, Blanchet FG, Byholm P (2021) The Ghost of the Hawk: top predator shaping bird communities in space and time. Front Ecol Evol 9:293. https://doi.org/10.3389/fevo.2021.638039
Chalfoun AD, Schmidt KA (2012) Adaptive breeding-habitat selection: Is it for the birds? Auk 129:589–599. https://doi.org/10.1525/auk.2012.129.4.589
Clark KL, Robertson RJ (1979) Spatial and temporal multi-species nesting aggregations in birds as anti-parasite and anti-predator defenses. Behav Ecol Sociobiol 5:359–371. https://doi.org/10.1007/BF00292524
Colorado GJ (2013) Why animals come together, with the special case of mixed-species bird flocks. Rev EIA 10:49–66
Danchin E, Giraldeau L-A, Valone TJ, Wagner RH (2004) Public information: from nosy neighbors to cultural evolution. Science 305(5683):487–491. https://doi.org/10.1126/science.1098254
Davies NB (2000) Cuckoos, Cowbirds and Other Cheats. Poyser, London, UK
Davies NB, Welbergen JA (2008) Cuckoo-hawk mimicry? An experimental test. Proc R Soc B Biol Sci 275:1817–1822. https://doi.org/10.1098/rspb.2008.0331
Doligez B, Cadet C, Danchin E, Boulinier T (2003) When to use public information for breeding habitat selection? The role of environmental predictability and density dependence. Anim Behav 66:973–988. https://doi.org/10.1006/anbe.2002.2270
Doligez B, Danchin E, Clobert J (2002) Public information and breeding habitat selection in a wild bird population. Science 297:1168–1170. https://doi.org/10.1126/science.1072838
Expósito-Granados M, Parejo D, Martínez JG et al (2017) Host nest site choice depends on risk of cuckoo parasitism in magpie hosts. Behav Ecol 28:1492–1497. https://doi.org/10.1093/beheco/arx113
Feeney WE, Medina I, Somveille M et al (2013) Brood parasitism and the evolution of cooperative breeding in birds. Science 342:1506–1508. https://doi.org/10.1126/science.1240039
Feeney WE, Welbergen JA, Langmore NE (2012) The frontline of avian brood parasite-host coevolution. Anim Behav 84:3–12. https://doi.org/10.1016/j.anbehav.2012.04.011
Forsman JT, Martin TE (2009) Habitat selection for parasite-free space by hosts of parasitic cowbirds. Oikos 118:464–470. https://doi.org/10.1111/j.1600-0706.2008.17000.x
Forsman JT, Mönkkönen M (2001) Responses by breeding birds to heterospecific song and mobbing call playbacks under varying predation risk. Anim Behav 62:1067–1073. https://doi.org/10.1006/anbe.2001.1856
Forsman JT, Mönkkönen M, Helle P, Inkeröinen J (1998) Heterospecific attraction and food resources in migrants’ breeding patch selection in northern boreal forest. Oecologia 115:278–286. https://doi.org/10.1007/s004420050517
Forsman JT, Seppänen JT (2011) Learning what (not) to do: Testing rejection and copying of simulated heterospecific behavioural traits. Anim Behav 81:879–883. https://doi.org/10.1016/j.anbehav.2011.01.029
Forsman JT, Seppänen JT, Mönkkönen M (2002) Positive fitness consequences of interspecific interaction with a potential competitor. Proc R Soc B Biol Sci 269:1619–1623. https://doi.org/10.1098/rspb.2002.2065
Gluckman TL, Mundy NI (2013) Cuckoos in raptors’ clothing: Barred plumage illuminates a fundamental principle of Batesian mimicry. Anim Behav 86:1165–1181. https://doi.org/10.1016/j.anbehav.2013.09.020
Goodenough AE, Elliot SL, Hart AG (2009) Are nest sites actively chosen? Testing a common assumption for three non-resource limited birds. Acta Oecologica 35:598–602. https://doi.org/10.1016/j.actao.2009.05.003
Gotmark F, Post P (1996) Prey selection by sparrowhawks, Accipiter nisus: relative predation risk for breeding passerine birds in relation to their size, ecology and behaviour. Philos Trans R Soc London Ser B Biol Sci 351:1559–1577. https://doi.org/10.1098/RSTB.1996.0141
Grim T (2008) Are Blackcaps (Sylvia atricapilla) defending their nests also calling for help from their neighbours? J Ornithol 149:169–180. https://doi.org/10.1007/s10336-007-0257-7
Grim T, Rutila J, Cassey P, Hauber ME (2009) The cost of virulence: an experimental study of egg eviction by brood parasitic chicks. Behav Ecol 20:1138–1146. https://doi.org/10.1093/beheco/arp108
Grim T, Samaš P, Procházka P, Rutila J (2014) Are tits really unsuitable hosts for the common Cuckoo? Ornis Fenn 91:166–177
Hartig F (2018) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R package version 0.2.0. https://CRAN.R-project.org/package=DHARMa
Hurd CR (1996) Interspecific attraction to the mobbing calls of black-capped chickadees (Parus atricapillus). Behav Ecol Sociobiol 38:287–292. https://doi.org/10.1007/s002650050244
Kelly JK, Suckow NM, Ward MP (2019) Preferential settling at sites with higher conspecific density does not protect Yellow Warblers (Setophaga petechia) from brood parasitism. Acta Oecol 96:24–28. https://doi.org/10.1016/j.actao.2019.03.003
Krüger O (2007) Cuckoos, cowbirds and hosts: adaptations, trade-offs and constraints. Philos Trans R Soc B Biol Sci 362:1873–1886. https://doi.org/10.1098/rstb.2006.1849
Lehtonen TK, Lindström K, Wong BBM (2013) Effect of egg predator on nest choice and nest construction in sand gobies. Anim Behav 86:867–871. https://doi.org/10.1016/j.anbehav.2013.08.005
Li D, Wei H, Zhang Z et al (2015) Oriental reed warbler (Acrocephalus orientalis) nest defence behaviour towards brood parasites and nest predators. Behaviour 152:1601–1621. https://doi.org/10.1163/1568539X-00003295
Liang W, Møller AP, Stokke BG et al (2016) Geographic variation in egg ejection rate by great tits across 2 continents. Behav Ecol 27:1405–1412. https://doi.org/10.1093/beheco/arw061
Lima SL (2009) Predators and the breeding bird: Behavioral and reproductive flexibility under the risk of predation. Biol Rev 84:485–513
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. Am Nat 153:649–659. https://doi.org/10.1086/303202
Loukola OJ, Seppänen JT, Forsman JT (2012) Intraspecific social information use in the selection of nest site characteristics. Anim Behav 83:629–633. https://doi.org/10.1016/j.anbehav.2011.12.004
Ma L, Yang C, Liang W (2018a) Hawk mimicry does not reduce attacks of cuckoos by highly aggressive hosts. Avian Res 9:35. https://doi.org/10.1186/s40657-018-0127-4
Ma L, Yang C, Liu J et al (2018b) Costs of breeding far away from neighbors: Isolated host nests are more vulnerable to cuckoo parasitism. Behav Processes 157:327–332. https://doi.org/10.1016/j.beproc.2018.07.017
Marti CD, Korpimäki E, Jaksić FM (1993) Trophic Structure of Raptor Communities: A Three-Continent Comparison and Synthesis. Current Ornithology. Springer, US, Boston, MA, pp 47–137
Martin TE (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127. https://doi.org/10.2307/2937160
Martin TE (1993) Nest Predation and Nest Sites. Bioscience 43:523–532. https://doi.org/10.2307/1311947
Mayor SJ, Schneider DC, Schaefer JA, Mahoney SP (2009) Habitat selection at multiple scales. Ecoscience 16:238–247. https://doi.org/10.2980/16-2-3238
Mönkkönen M, Forsman JT (2002) Heterospecific attraction among forest birds: a review. Ornithol Sci 1:41–51. https://doi.org/10.2326/osj.1.41
Mönkkönen M, Helle P, Soppela K (1990) Numerical and behavioural responses of migrant passerines to experimental manipulation of resident tits (Parus spp.): heterospecific attraction in northern breeding bird communites? Oecologia 85:218–225. https://doi.org/10.1007/BF00319404
Mönkkönen M, Husby M, Tornberg R et al (2007) Predation as a landscape effect: The trading off by prey species between predation risks and protection benefits. J Anim Ecol 76:619–629. https://doi.org/10.1111/j.1365-2656.2007.01233.x
Moreras A, Tolvanen J, Morosinotto C et al (2021) Choice of nest attributes as a frontline defense against brood parasitism. Behav Ecol 32:1285–1295. https://doi.org/10.1093/beheco/arab095
Morosinotto C, Thomson RL, Hänninen M, Korpimäki E (2012) Higher nest predation risk in association with a top predator: Mesopredator attraction? Oecologia 170:507–515. https://doi.org/10.1007/s00442-012-2320-1
Morris DW (2003) Toward an ecological synthesis: A case for habitat selection. Oecologia 136:1–13
Morse DH (1977) Feeding behavior and predator avoidance in heterospecific groups. Bioscience 27:332–339. https://doi.org/10.2307/1297632
Nielsen JT, Drachmann J (1999) Prey selection of Goshawks Accipiter gentilis during the breeding season in Vendsyssel, Denmark. Dansk Orn Foren Tidsskr 93:85–90
Nilsson SG (1984) The evolution of nest-site selection among hole-nesting birds: the importance of nest predation and competition. Ornis Scand 15:167–175. https://doi.org/10.2307/3675958
Nocera JJ, Forbes GJ, Giraldeau LA (2009) Aggregations from using inadvertent social information: A form of ideal habitat selection. Ecography (cop) 32:143–152. https://doi.org/10.1111/j.1600-0587.2008.05614.x
Parejo D, Danchin E, Avilés JM (2005) The heterospecific habitat copying hypothesis: can competitors indicate habitat quality? Behav Ecol 16:96–105. https://doi.org/10.1093/BEHECO/ARH136
Perperoglou A, Sauerbrei W, Abrahamowicz M (2019) Schmid M (2019) A review of spline function procedures in R. BMC Med Res Methodol 191(19):1–16. https://doi.org/10.1186/S12874-019-0666-3
Pizzatto L, Stockwell M, Clulow S et al (2016) Finding a place to live: conspecific attraction affects habitat selection in juvenile green and golden bell frogs. Acta Ethol 19:1–8. https://doi.org/10.1007/s10211-015-0218-8
Polak M (2014) Protective nesting association between the Barred Warbler Sylvia nisoria and the Red-backed Shrike Lanius collurio: an experiment using artificial and natural nests. Ecol Res 29:949–957. https://doi.org/10.1007/s11284-014-1183-9
Quinn JL, Kokorev Y (2002) Trading-off risks from predators and from aggressive hosts. Behav Ecol Sociobiol 51:455–460. https://doi.org/10.1007/s00265-002-0466-2
Quinn JL, Ueta M (2008) Protective nesting associations in birds. Ibis 150:146–167. https://doi.org/10.1111/j.1474-919X.2008.00823.x
R Development Core Team (2019) A Language and Environment for Statistical Computing. R Found Stat Comput https://www.R-project.org
Rebollo S, García-Salgado G, Pérez-Camacho L et al (2017) Prey preferences and recent changes in diet of a breeding population of the Northern Goshawk Accipiter gentilis in Southwestern Europe. Bird Study 64:464–475. https://doi.org/10.1080/00063657.2017.1395807
Reed JM, Boulinier T, Danchin E, Oring LW (1999) Informed dispersal. Curr Ornithol. https://doi.org/10.1007/978-1-4757-4901-4_5
Reynolds JD (1996) Animal breeding systems. Trends Ecol Evol 11:68–72. https://doi.org/10.1016/0169-5347(96)81045-7
Richards SA, Whittingham MJ, Stephens PA (2011) Model selection and model averaging in behavioural ecology: The utility of the IT-AIC framework. Behav Ecol Sociobiol 65:77–89. https://doi.org/10.1007/s00265-010-1035-8
Rosenzweig ML (1981) A theory of habitat selection. Ecology 62:327–335. https://doi.org/10.2307/1936707
Rutila J, Latja R, Koskela K (2002) The common cuckoo Cuculus canorus and its cavity nesting host, the redstart Phoenicurus phoenicurus: A peculiar cuckoo-host system? J Avian Biol 33:414–419. https://doi.org/10.1034/j.1600-048X.2002.02937.x
Samaš P, Rutila J, Grim T (2016) The common redstart as a suitable model to study cuckoo-host coevolution in a unique ecological context. BMC Evol Biol 16:1–13. https://doi.org/10.1186/s12862-016-0835-5
Samplonius JM, Both C (2019) Climate change may affect fatal competition between two bird species. Curr Biol 29:327-331.e2. https://doi.org/10.1016/j.cub.2018.11.063
Seppänen JT, Forsman JT, Monkkönen M, Thomson RL (2007) Social information use is a process across time, space, and ecology, reaching heterospecifics. Ecology 88:1622–1633. https://doi.org/10.1890/06-1757.1
Sieving KE, Contreras TA, Maute KL (2004) Heterospecific facilitation of forest-boundary crossing by mobbing understory birds in north-central Florida. Auk 121:738–751. https://doi.org/10.2307/4090311
Solonen T, Lokki H, Sulkava S (2019) Diet and brood size in rural and urban Northern Goshawks Accipiter gentilis in southern Finland. Avian Biol Res 12:3–9. https://doi.org/10.1177/1758155919826754
Szymkowiak J (2013) Facing uncertainty: how small songbirds acquire and use social information in habitat selection process? Springer Sci Rev 1:115–131. https://doi.org/10.1007/s40362-013-0012-9
Szymkowiak J, Thomson RL, Kuczyński L (2016) Wood warblers copy settlement decisions of poor quality conspecifics: support for the tradeoff between the benefit of social information use and competition avoidance. Oikos 125:1561–1569. https://doi.org/10.1111/oik.03052
Thomson RL, Forsman JT, Mönkkönen M (2003) Positive interactions between migrant and resident birds: Testing the heterospecific attraction hypothesis. Oecologia 134:431–438. https://doi.org/10.1007/s00442-002-1140-0
Thomson RL, Forsman JT, Mönkkönen M (2011) Risk taking in natural predation risk gradients: Support for risk allocation from breeding pied flycatchers. Anim Behav 82:1443–1447. https://doi.org/10.1016/j.anbehav.2011.09.029
Thomson RL, Forsman JT, Sardà-Palomera F, Mönkkönen M (2006) Fear factor: Prey habitat selection and its consequences in a predation risk landscape. Ecography (cop) 29:507–514. https://doi.org/10.1111/j.0906-7590.2006.04568.x
Thomson RL, Tolvanen J, Forsman JT (2016) Cuckoo parasitism in a cavity nesting host: Near absent egg-rejection in a northern redstart population under heavy apparent (but low effective) brood parasitism. J Avian Biol 47:363–370. https://doi.org/10.1111/jav.00915
Tolvanen J, Forsman JT, Thomson RL (2017a) Reducing cuckoo parasitism risk via informed habitat choices. Auk 134:553–563. https://doi.org/10.1642/auk-17-30.1
Tolvanen J, Morosinotto C, Forsman JT, Thomson RL (2020) Information collected during the post-breeding season guides future breeding decisions in a migratory bird. Oecologia 192:965–977. https://doi.org/10.1007/s00442-020-04629-5
Tolvanen J, Pakanen VM, Valkama J, Tornberg R (2017b) Apparent survival, territory turnover and site fidelity rates in Northern Goshawk Accipiter gentilis populations close to the northern range limit. Bird Study 64:168–177. https://doi.org/10.1080/00063657.2017.1309351
Tornberg R, Mönkkönen M, Kivelä SM (2009) Landscape and season effects on the diet of the Goshawk. Ibis 151:396–400. https://doi.org/10.1111/j.1474-919X.2009.00910.x
Tornberg R, Rytkönen S, Välimäki P et al (2015) Northern Goshawk (Accipiter gentilis) may improve Black Grouse breeding success. J Ornithol 1571(157):363–370. https://doi.org/10.1007/S10336-015-1292-4
Toyne EP (1998) Breeding season diet of the Goshawk Accipiter gentilis in Wales. Ibis 140:569–579. https://doi.org/10.1111/j.1474-919x.1998.tb04701.x
Trnka A, Grim T (2013) Color plumage polymorphism and predator mimicry in brood parasites. Front Zool 10:25. https://doi.org/10.1186/1742-9994-10-25
Trnka A, Prokop P (2012) The effectiveness of hawk mimicry in protecting cuckoos from aggressive hosts. Anim Behav 83:263–268. https://doi.org/10.1016/j.anbehav.2011.10.036
Ueta M (2007) Effect of Japanese lesser sparrowhawks Accipiter gularis on the nest site selection of azure-winged magpies Cyanopica cyana through their nest defending behavior. J Avian Biol 38:427–431. https://doi.org/10.1111/j.2007.0908-8857.04172.x
Ueta M (1999) Cost of nest defense in azure-winged magpies. J Avian Biol 30:326. https://doi.org/10.2307/3677361
Valone TJ (2007) From eavesdropping on performance to copying the behavior of others: A review of public information use. Behav Ecol Sociobiol 62:1–14
Valtonen A, Latja R, Leinonen R, Pöysä H (2017) Arrival and onset of breeding of three passerine birds in eastern Finland tracks climatic variation and phenology of insects. J Avian Biol 48:785–795. https://doi.org/10.1111/JAV.01128
Van Balen JH, Booy CJH, Van Franeker JA, Osieck ER (1982) Studies on hole-nesting birds in natural nest sites. Ardea 70:1–24. https://doi.org/10.5253/arde.v70.p1
Welbergen JA, Davies NB (2011) A parasite in wolf’s clothing: Hawk mimicry reduces mobbing of cuckoos by hosts. Behav Ecol 22:574–579. https://doi.org/10.1093/beheco/arr008
Wesołowski T (2002) Anti-predator adaptations in nesting Marsh Tits Parus palustris: The role of nest-site security. Ibis 144:593–601. https://doi.org/10.1046/j.1474-919X.2002.00087.x
Wood SN (2017) Generalized additive models: an introduction with R, 2nd edn. Chapman and Hall/CRC, New York. https://doi.org/10.1201/9781315370279
Zuur AF, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Stat Biol Health. https://doi.org/10.1007/978-0-387-87458-6
Acknowledgements
We appreciate the help in field work of Claire Buchan, Felicitas Pamatat, Guilia Masoero, Selengemurun Dembereldagva, Verity Bridger, Carles Durà, Victoria Pritchard, Mikko Karjalainen and Ryan Miller during various years of data collection. We also want to thank the anonymous reviewers, given that their comments improve our manuscript.
Funding
Funding was provided by a DST-NRF Centre of Excellence of South Africa, Academy of Finland (grants no. 12265 and 125720 to JTF, and grant no. 138049 to RLT), Kone Foundation (to JTF and JT), Kvantum Institute, Societas pro Fauna et Flora Fennica and Oskar Öflunds Stiftelse (to JT).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All animal experiments were approved by the Finnish Center for Economics Development, Transport and Environment (Elinkeino-liikenne-ja ympäristökeskus, ELY, permit numbers: POPELY/136/07.01/2014 and VARELY/921/2017).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Andreas Nord.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Moreras, A., Tolvanen, J., Tornberg, R. et al. Breeding near heterospecifics as a defence against brood parasites: can redstarts lower probability of cuckoo parasitism using neighbours?. Oecologia 199, 871–883 (2022). https://doi.org/10.1007/s00442-022-05242-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-022-05242-4