BACKGROUND: Co-evolutionary arms-races result in spatio-temporally dynamic relationships between interacting species, e.g., brood parasites and their avian hosts. However, majority of avian co-evolutionary studies are limited to "snap-shots" of a single breeding season in an open-nesting host. In a long-term study (11 breeding seasons), we explored a unique system between the brood parasitic common cuckoo (Cuculus canorus) and its host, the common redstart (Phoenicurus phoenicurus) which is exceptional among all cuckoo hosts due to being a cavity nester. Conditions in cavities are different from open nests, e.g., lower risks of predation, more favourable microclimate, increased risks of unsuccessful eviction of host offspring by the cuckoo nestling. Different conditions in cavities thus can be expected to shape parasite-host coevolution differently from what is typically studied in open nesting hosts. RESULTS: In our highly parasitised nest-box population (32.5%, n = 569 nests) only 35.7% of cuckoo eggs were laid into the nest cup and incubated by redstarts. Host nests shifted availability to later into the breeding season from 2006 to 2016 and cuckoos followed this trend by also shifting their timing of parasitism. Although previous studies revealed that redstarts selectively eject experimental non-mimetic eggs (desertion was not a specific response to foreign eggs), the hosts never ejected naturally-laid cuckoo eggs or cuckoo eggs cross-fostered into naturally non-parasitised nests. We solve the long-standing debate about the origin of cuckoo eggs found on the nest rim: we gained the first direct video-recording evidence that eggs found on the nest rim were mislaid by parasites and not ejected by hosts. Naturally-parasitised nests were deserted more often (18.6%) than control non-parasitized nests (5.6%) or nests artificially parasitised by us (1.4%). This suggests that the sight of the laying cuckoo female is the primary cue that triggers egg rejection (by desertion) in this host. Review of data from this and other study sites (10 populations, n = 853 experiments) demonstrates high variability in rejection rates and shows that populations facing higher parasitism rates reject parasitic eggs with higher frequencies. Surprisingly, cuckoo chicks either growing solitarily or with redstart chicks did not differ in their fledging success. CONCLUSIONS: We suggest that the redstart is an ideal model system to study the flexibility and limits of brood parasite-host co-evolution in an extreme ecological setting.

Department of Zoology and Laboratory of Ornithology Palacky University 17 listopadu 50 Olomouc 77146 Czech Republic

Kannelkatu 5 as 26 Lappeenranta Finland

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Feeney WE, Welbergen JA, Langmore NE. Advances in the study of coevolution between avian brood parasites and their hosts. Annu Rev Ecol Evol Syst. 2014;45:227–246. doi: 10.1146/annurev-ecolsys-120213-091603. DOI

Dawkins R, Krebs JR. Arms races between and within species. Proc R Soc Lond B. 1979;205:489–511. doi: 10.1098/rspb.1979.0081. PubMed DOI

Takasu F. Why do all host species not show defense against avian brood parasitism: evolutionary lag or equilibrium? Am Nat. 1998;151:193–205. doi: 10.1086/286111. PubMed DOI

Davies NB. Cuckoos, cowbirds and other cheats. London: T. & A. D. Poyser; 2000.

Davies NB, Brooke ML. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol. 1989;58:207–224. doi: 10.2307/4995. DOI

Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe H, Pedersen HC. Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour. 1991;116:64–89. doi: 10.1163/156853990X00365. DOI

Grim T, Samaš P, Moskát C, Kleven O, Honza M, Moksnes A, Røskaft E, Stokke BG. Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts? J Anim Ecol. 2011;80:508–518. doi: 10.1111/j.1365-2656.2010.01798.x. PubMed DOI

Kleven O, Moksnes A, Røskaft E, Rudolfsen G, Stokke BG, Honza M. Breeding success of common cuckoos Cuculus canorus parasitising four sympatric species of Acrocephalus warblers. J Avian Biol. 2004;35:394–398. doi: 10.1111/j.0908-8857.2004.03359.x. DOI

Vogl W, Taborsky B, Taborsky M, Teuschl Y, Honza M. Habitat and space use of European cuckoo females during the egg laying period. Behaviour. 2004;141:881–898. doi: 10.1163/1568539042265671. DOI

Stokke BG, Hafstad I, Rudolfsen G, Bargain B, Beier J, Campas DB, Dyrcz A, Honza M, Leisler B, Pap PL, Patapavičius R, Procházka P, Schulze-Hagen K, Thomas R, Moksnes A, Møller AP, Røskaft E, Soler M. Host density predicts presence of cuckoo parasitism in reed warblers. Oikos. 2007;116:913–922. doi: 10.1111/j.0030-1299.2007.15832.x. DOI

Stokke BG, Hafstad I, Rudolfsen G, Moksnes A, Møller AP, Røskaft E, Soler M. Predictors of resistance to brood parasitism within and among reed warbler populations. Behav Ecol. 2008;19:612–620. doi: 10.1093/beheco/arn007. DOI

Anderson MG, Moskát C, Bán M, Grim T, Cassey P, Hauber ME. Egg eviction imposes a recoverable cost of virulence in chicks of a brood parasite. PLoS ONE. 2009;4:e7725. doi: 10.1371/journal.pone.0007725. PubMed DOI PMC

Antonov A, Stokke BG, Moksnes A, Røskaft E. Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host. Biol Lett. 2009;5:169–171. doi: 10.1098/rsbl.2008.0645. PubMed DOI PMC

Trnka A, Prokop P, Grim T. Uncovering dangerous cheats: how do avian hosts recognize adult brood parasites? PLoS ONE. 2012;7:e37445. doi: 10.1371/journal.pone.0037445. PubMed DOI PMC

Davies NB, Brooke ML, Kacelnik A. Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proc R Soc Lond B. 1996;263:925–931. doi: 10.1098/rspb.1996.0137. DOI

Rutila J, Latja R, Koskela K. The common cuckoo

Igic B, Cassey P, Grim T, Greenwood DR, Moskát C, Rutila J, Hauber ME. A shared chemical basis of avian host–parasite egg colour mimicry. Proc R Soc B. 2012;279:1068–1076. doi: 10.1098/rspb.2011.1718. PubMed DOI PMC

Fossøy F, Sorenson MD, Liang W, Ekrem T, Moksnes A, Møller AP, Rutila J, Røskaft E, Takasu F, Yang C, Stokke BG. Ancient origin and maternal inheritance of blue cuckoo eggs. Nat Commun. 2016;7:10272. doi: 10.1038/ncomms10272. PubMed DOI PMC

Haikola J, Rutila J. Käki. Otava: Helsinki; 2008.

Capek V. Beiträge zur fortpflanzungsgeschichte des Kuckucks. Orn Jahrb. 1896;7:41–72,102–117,146–157,165–183.

Grim T, Rutila J, Cassey P, Hauber ME. The cost of virulence: an experimental study of egg eviction by brood parasitic chicks. Behav Ecol. 2009a;20:1138–46.

Grim T, Rutila J, Cassey P, Hauber ME. Experimentally constrained virulence is costly for common cuckoo chicks. Ethology. 2009b;115:14–22.

Avilés JM, Rutila J, Møller AP. Should the redstart Phoenicurus phoenicurus accept or reject cuckoo Cuculus canorus eggs? Behav Ecol Sociobiol. 2006;58:608–617. doi: 10.1007/s00265-005-0941-7. DOI

Thomson RL, Tolvanen J, Forsman JT. 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. 2016;47:363–370. doi: 10.1111/jav.00915. DOI

Rutila J, Jokimäki J, Avilés JM, Kaisanlahti-Jokimäki ML. Responses of parasitized and unparasitized common redstart (Phoenicurus phoenicurus) populations against artificial cuckoo parasitism. Auk. 2006;123:259–265. doi: 10.1642/0004-8038(2006)123[0259:ROPAUC]2.0.CO;2. DOI

Johnson DH. The importance of replication in wildlife research. J Wildl Manage. 2002;66:919–932. doi: 10.2307/3802926. DOI

Kelly CD. Replicating empirical research in behavioral ecology: how and why it should be done but rarely ever is. Q Rev Biol. 2006;81:221–236. doi: 10.1086/506236. PubMed DOI

Samas P, Hauber ME, Cassey P, Grim T. Host responses to interspecific brood parasitism: a by-product of adaptation to conspecific parasitism? Front Zool. 2014;11:34. doi: 10.1186/1742-9994-11-34. PubMed DOI PMC

Soler JJ, Martínez JG, Soler M, Møller AP. Genetic and geographic variation in rejection behavior of cuckoo eggs by European magpie populations: an experimental test of rejecter-gene flow. Evolution. 1999;53:947–956. doi: 10.2307/2640734. PubMed DOI

Hurlbert SH. Pseudoreplication and the design of ecological field experiments. Ecol Monogr. 1984;54:187–211. doi: 10.2307/1942661. DOI

The Finnish Meteorological Institute 2016. https://en.ilmatieteenlaitos.fi/open-data. Accessed 15 Sept 2016.

Dinets V, Samaš P, Croston R, Grim T, Hauber ME. Predicting the responses of native birds to transoceanic invasions by avian brood parasites. J Field Ornithol. 2015;86:244–251. doi: 10.1111/jofo.12111. DOI

Samaš P, Cassey P, Hauber ME, Grim T. Repeatability of foreign egg rejection: testing the assumptions of co-evolutionary theory. Ethology. 2011;117:606–619. doi: 10.1111/j.1439-0310.2011.01917.x. DOI

Hauber ME, Samaš P, Anderson MG, Rutila J, Low J, Cassey P, Grim T. Life-history theory predicts host behavioural responses to experimental brood parasitism. Ethol Ecol Evol. 2014;26:349–364. doi: 10.1080/03949370.2013.851121. DOI

Grim T. Are cavity nesters really unsuitable hosts for the common cuckoo (Cuculus canorus)? An experiment with the blue tit (Cyanistes caeruleus) and collared flycatcher (Ficedula albicollis) Sylvia. 2016;52:37–50.

Hanley D, Samaš P, Heryán J, Hauber ME, Grim T. Now you see it, now you don’t: flushing hosts prior to experimentation can predict their responses to brood parasitism. Sci Rep. 2015;5:9060. doi: 10.1038/srep09060. PubMed DOI PMC

Grim T. Mimicry vs. similarity: which resemblances between brood parasites and their hosts are mimetic and which are not? Biol J Linn Soc. 2005;84:69–78. doi: 10.1111/j.1095-8312.2005.00414.x. DOI

Forstmeier W, Schielzeth H. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol. 2011;65:47–55. doi: 10.1007/s00265-010-1038-5. PubMed DOI PMC

Grafen A, Hails R. Modern Statistics for the Life Sciences. Oxford: Oxford University Press; 2002.

Zuur AF, Ieno EN, Elphick C. A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol. 2010;1:3–14. doi: 10.1111/j.2041-210X.2009.00001.x. DOI

R Core Team 2014. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/. Accessed 15 Sept 2016.

von Haartman L. The reaction of a regular cuckoo host to foreign eggs. Ornis Fenn. 1976;53:96–98.

Järvinen A. Relationship between the common cuckoo Cuculus canorus and its host, the redstart Phoenicurus phoenicurus. Ornis Fenn. 1984;61:84–88.

Grim T, Samaš P, Procházka P, Rutila J. Are tits really unsuitable hosts for the common cuckoo? Ornis Fenn. 2014;91:166–177.

Berkowic D, Stokke BG, Meiri S, Markman S. Climate change and coevolution in the cuckoo–reed warbler system. Evol Ecol. 2015;29:581–597. doi: 10.1007/s10682-015-9763-x. DOI

Moksnes A, Røskaft E, Hagen LG, Honza M, Mørk C, Olsen PH. Common cuckoo Cuculus canorus and host behaviour at reed warbler Acrocephalus scirpaceus nests. Ibis. 2000;142:247–258. doi: 10.1111/j.1474-919X.2000.tb04864.x. DOI

Polačiková L, Grim T. Blunt egg pole holds cues for alien egg discrimination: experimental evidence. J Avian Biol. 2010;41:111–6. doi: 10.1111/j.1600-048X.2010.04983.x. DOI

Lagerström M. Käki, Cuculus canorus. In: Hyytiä K, Kellomäki E, Koistinen J, editors. Suomen lintuatlas. Helsinki: SLY:n Lintutieto Oy; 1983. pp. 238–239.

Wyllie I. The cuckoo. London: Batsford; 1981.

von Haartman L. Co-evolution of the cuckoo Cuculus canorus and a regular cuckoo host. Ornis Fenn. 1981;58:1–10.

Cross-continental test of natal philopatry and habitat-imprinting hypotheses to explain host specificity in an obligate brood parasite

Rearing a virulent common cuckoo is not extra costly for its only cavity-nesting host