Abstract
In some populations of the host of brood parasites, more than two parasite eggs may be laid in a single nest. This phenomenon is known as multiple parasitism, representing a cost to both the host and parasite. In this study, we analysed a long-term dataset (2007–2021) focusing on multiple parasitism of the common cuckoo (Cuculus canorus) parasitizing the great reed warbler (Acrocephalus arundinaceus). The annual parasitism rate was on average 54.3% and varied between 5.8% and 92.2%, depending on the year. Out of 720 parasitized nests, double parasitism was recorded in 172 (23.9%) nests, triple in 51 (7.1%) nests, quadruple in 10 (1.3%) nests, and, exceptionally, in the years of heavy parasitism (about 90%), quintuple parasitism was recorded in three (0.4%) nests. The rate of multiple parasitism ranged from 0 to 63% inter-annually and strongly correlated with the parasitism rate and the total number of parasite eggs found. Furthermore, the number of cuckoo eggs laid per one nest increased with the decreasing daily availability of host nests that were at a suitable breeding stage for parasitism. Both genetic and egg phenotype analyses revealed that no cuckoo female laid more than one egg in the same host nest. Using data on long-term parasite–host interactions and from continuous video recording, as well as progressive methods to assign parasite offspring thus helped us better understand various aspects of multiple parasitism in hosts heavily parasitized by an evictor brood parasite.
Significance statement
Laying more parasite eggs in one host nest (i.e. multiple parasitism) is common in brood parasites whose nestlings share the nest with nestmates. In the species where the parasite’s nestling kills its nest mates, multiple parasitism should be rare because it is costly for the parasite. However, in host populations with high parasitism rates, multiple parasitism occurs more often than predicted. Using long-term and video-recording data, we quantified multiple parasitism in the common cuckoo across years and host egg-laying sequences. We found that the rate of multiple parasitism is positively related to the parasitism rate and that the lower the number of nests suitable for parasitism, the higher the number of parasite eggs in one nest. Based on genetic and egg phenotype analyses, we also showed that individual parasitic females avoid laying in the nests they had already parasitized.
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Data availability
The datasets generated and/or analysed during the current study are available from the supplementary information file.
References
Antonov A, Stokke BG, Moksnes A, Røskaft E (2006) Egg rejection in marsh warblers (Acrocephalus palustris) heavily parasitized by common cuckoos (Cuculus canorus). Auk 123:419–430. https://doi.org/10.1093/auk/123.2.419
Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Brooker LC, Brooker MG (1990) Why are cuckoos host specific? Oikos 57:301–309
Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3-Genes Genom Genet 1:171–182. https://doi.org/10.1534/g3.111.000240
Chance EP (1940) The truth about the cuckoo. Country Life, London
Davies NB (2000) Cuckoos, cowbirds and other cheats. T. & A. D, Poyser, London
de la Colina MA, Hauber ME, Strausberger BM, Reboreda JC, Mahler B (2016) Molecular tracking of individual host use in the Shiny Cowbird – a generalist brood parasite. Ecol Evol 6:4684–4696. https://doi.org/10.1002/ece3.2234
De Mársico MC, Reboreda JC (2014) High frequency but low impact of brood parasitism by the specialist screaming cowbird on its primary host, the baywing. Emu 114:309–316. https://doi.org/10.1071/MU14008
De Mársico MC, Gloag R, Ursino CA, Reboreda JC (2013) A novel method of rejection of brood parasitic eggs reduces parasitism intensity in a cowbird host. Biol Lett 9:20130076. https://doi.org/10.1098/rsbl.2013.0076
Ellison K, Sealy SG, Gibbs HL (2006) Genetic elucidation of host use by individual sympatric bronzed cowbirds (Molothrus aeneus) and brown-headed cowbirds (M. ater). Can J Zool 84:1269–1280. https://doi.org/10.1139/z06-091
Fossøy F, Antonov A, Moksnes A, Røskaft E, Vikan JR, Møller AP, Shykoff JA, Stokke BG (2011) Genetic differentiation among sympatric cuckoo host races: males matter. Proc R Soc B 278:1639–1645. https://doi.org/10.1098/rspb.2010.2090
Fossøy F, Moksnes A, Røskaft E, Antonov A, Dyrcz A, Moskát C, Ranke PS, Rutila J, Vikan JR, Stokke BG (2012) Sex allocation in relation to host races in the brood-parasitic common cuckoo (Cuculus canorus). PLoS ONE 7:e36884. https://doi.org/10.1371/journal.pone.0036884
Geltsch N, Bán M, Hauber ME, Moskát C (2016) When should common cuckoos Cuculus canorus lay their eggs in host nests? Bird Study 63:46–51. https://doi.org/10.1080/00063657.2015.1125851
Gibbs HL, Sorenson MD, Marchetti K, de Brooke ML, Davies N, Nakamura H (2000) Genetic evidence for female host-specific races of the common cuckoo. Nature 407:183. https://doi.org/10.1038/35025058
Gloag R, Fiorini VD, Reboreda JC, Kacelnik A (2013) The wages of violence: mobbing by mockingbirds as a frontline defence against brood parasitic cowbirds. Anim Behav 86:1023–1029. https://doi.org/10.1016/j.anbehav.2013.09.007
Gloag R, Fiorini VD, Reboreda JC, Kacelnik A (2014a) Shiny cowbirds share foster mothers but not true mothers in multiply parasitized mockingbird nests. Behav Ecol Sociobiol 68:681–689. https://doi.org/10.1007/s00265-014-1682-2
Gloag R, Keller LA, Langmore NE (2014b) Cryptic cuckoo eggs hide from competing cuckoos. Proc R Soc B 281:20141014. https://doi.org/10.1098/rspb.2014.1014
Goguen CB, Curson DR, Mathews NE (2011) Costs of multiple parasitism for an avian brood parasite, the brown-headed cowbird (Molothrus ater). Can J Zool 89:1237–1248. https://doi.org/10.1139/Z11-104
Gómez J, Gordo O, Minias P (2021) Egg recognition: the importance of quantifying multiple repeatable features as visual identity signals. PLoS ONE 16:e0248021. https://doi.org/10.1371/journal.pone.0248021
Honza M, Taborsky B, Taborsky M, Teuschl Y, Vogl W, Moksnes A, Røskaft E (2002) Behaviour of female common cuckoos, Cuculus canorus, in the vicinity of host nests before and during egg laying: a radiotelemetry study. Anim Behav 64:861–868. https://doi.org/10.1093/beheco/arw085
Honza M, Šulc M, Jelínek V, Požgayová M, Procházka P (2014) Brood parasites lay eggs matching the appearance of host clutches. Proc R Soc B 281:20132665. https://doi.org/10.1098/rspb.2013.2665
Honza M, Požgayová M, Procházka P, Koleček J (2020) Errors in egg laying by female common cuckoo Cuculus canorus in nests of its common host. Ibis 162:637–644. https://doi.org/10.1111/ibi.12808
Hoover JP (2003) Multiple effects of brood parasitism reduce the reproductive success of prothonotary warblers, Protonotaria citrea. Anim Behav 65:923–934. https://doi.org/10.1006/anbe.2003.2155
Jelínek V, Procházka P, Požgayová M, Honza M (2013) Common cuckoos Cuculus canorus change their nest-searching strategy according to the number of available host nests. Ibis 156:189–197. https://doi.org/10.1111/ibi.12093
Jelínek V, Šulc M, Štětková G, Honza M (2021) Fast and furious: host aggression modulates behaviour of brood parasites. Ibis 163:824–833. https://doi.org/10.1111/ibi.12930
Johnson EW, McRae SB (2022) Interclutch variability in egg characteristics in two species of rail: Is maternal identity encoded in eggshell patterns? PLoS ONE 17:e0261868. https://doi.org/10.1371/journal.pone.0261868
Jones OR, Wang J (2010) Colony: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555. https://doi.org/10.1111/j.1755-0998.2009.02787.x
Kattan GH (1997) Shiny cowbirds follow the ‘shotgun’ strategy of brood parasitism. Anim Behav 53:647–654. https://doi.org/10.1006/anbe.1996.0339
Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Koleček J, Piálková R, Piálek L et al (2021) Spatiotemporal patterns of egg laying in the common cuckoo. Anim Behav 177:107–116. https://doi.org/10.1016/j.anbehav.2021.04.021
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Lea SE, Kattan GH (1998) Reanalysis gives further support to the ‘shotgun’ model of shiny cowbird parasitism of house wren nests. Anim Behav 56:1571–1573. https://doi.org/10.1006/anbe.1998.0925
Liu J, Yang C, Liang W (2019) Brood parasitism of rosefinches by cuckoos: suitable host or accidental parasitism? J Ethol 37:83–92. https://doi.org/10.1007/s10164-018-0571-y
Maia R, Gruson H, Endler JA, White TE (2019) Pavo 2: new tools for the spectral and spatial analysis of colour in R. Methods Ecol Evol 10:1097–1107. https://doi.org/10.1111/2041-210X.13174
Manly BFJ (1997) Monte Carlo methods. randomization, bootstrap, and Monte Carlo methods in biology, 2nd edn. Chapman and Hall, London, pp 69–78
Manna TJ, Moskát C, Tong L, Bán M, Aidala Z, Low J, Hauber ME (2019) Multiple parasitism reduces egg rejection in the host (Acrocephalus arundinaceus) of a mimetic avian brood parasite (Cuculus canorus). J Comp Psychol 133:351–358. https://doi.org/10.1037/com0000166
Martínez JG, Burke T, Dawson D, Soler JJ, Soler M, Møller AP (1998a) Microsatellite typing reveals mating patterns in the brood parasitic great spotted cuckoo (Clamator glandarius). Mol Ecol 7:289–297. https://doi.org/10.1046/j.1365-294X.1998.00348.x
Martínez JG, Soler JJ, Soler M, Burke T (1998b) Spatial pattern of egg laying and multiple parasitism in a brood parasite: a non-territorial system in the great spotted cuckoo (Clamator glandarius). Oecologia 117:286–294. https://doi.org/10.1007/s004420050660
Marton A (2021) Quintuple parasitism of a great reed warbler nest by common cuckoos. Ecol Evol 11:8420–8423. https://doi.org/10.1002/ece3.7669
Marton A, Fülöp A, Ozogány K, Moskát C, Bán M (2019) Host alarm calls attract the unwanted attention of the brood parasitic common cuckoo. Sci Rep 9:18563. https://doi.org/10.1038/s41598-019-54909-1
McLaren CM, Woolfenden BE, Gibbs HL, Sealy SG (2003) Temporal patterns of multiple parasitism by brown-headed cowbirds (Molothrus ater) on song sparrows (Melospiza melodia). Can J Zool 81:281–286. https://doi.org/10.1139/z03-002
Moksnes A, Røskaft E (1995) Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs from European museum collections. J Zool 236:625–648. https://doi.org/10.1111/j.1469-7998.1995.tb02736.x
Moksnes A, Røskaft E, Bičík V, Honza M, Øien IJ (1993) Cuckoo Cuculus canorus parasitism on Acrocephalus warblers in Southern Moravia in the Czech Republic. J Ornithol 134:425–434
Moksnes A, Røskaft E, Hagen LG, Honza M, Mørk C, Olsen PH (2000) Common cuckoo Cuculus canorus and host behaviour at reed warbler Acrocephalus scirpaceus nests. Ibis 142:247–258. https://doi.org/10.1111/j.1474-919X.2000.tb04864.x
Moksnes A, Røskaft E, Rudolfsen G et al (2008) Individual female common cuckoos Cuculus canorus lay constant egg types but egg appearance cannot be used to assign eggs to females. J Avian Biol 39:238–241. https://doi.org/10.1111/j.2008.0908-8857.04158.x
Moskát C, Honza M (2002) European cuckoo Cuculus canorus parasitism and host’s rejection behaviour in a heavily parasitized great reed warbler Acrocephalus arundinaceus population. Ibis 144:614–622. https://doi.org/10.1046/j.1474-919X.2002.00085.x
Moskát C, Barta Z, Hauber ME, Honza M (2006) High synchrony of egg laying in common cuckoos (Cuculus canorus) and their great reed warbler (Acrocephalus arundinaceus) hosts. Ethol Ecol Evol 18:159–167. https://doi.org/10.1080/08927014.2006.9522720
Moskát C, Hauber ME, Avilés JM, Bán M, Hargitai R, Honza M (2009) Increased host tolerance of multiple cuckoo eggs leads to higher fledging success of the brood parasite. Anim Behav 77:1281–1290. https://doi.org/10.1016/j.anbehav.2009.01.030
Nakamura H, Miyazawa Y (1997) Movements, space use and social organisation of radiotracked common cuckoos during the breeding season in Japan. Japn J Ornithol 46:23–54. https://doi.org/10.3838/jjo.46.23
Nakamura H, Miyazawa Y, Kashiwagi K (2005) Behavior of radio-tracked common cuckoo females during the breeding season in Japan. Ornithol Sci 4:31–41. https://doi.org/10.2326/osj.4.31
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7:e37135. https://doi.org/10.1371/journal.pone.0037135
Piálek L, Burress E, Dragová K, Almirón A, Casciotta J, Říčan O (2019) Phylogenomics of pike cichlids (Cichlidae: Crenicichla) of the C. mandelburgeri species complex: Rapid ecological speciation in the Iguazú river and high endemism in the Middle Paraná basin. Hydrobiologia 832:355–375. https://doi.org/10.1007/s10750-018-3733-6
Požgayová M, Procházka P, Honza M (2013) Is shared male assistance with antiparasitic nest defence costly in the polygynous great reed warbler? Anim Behav 85:615–621. https://doi.org/10.1016/j.anbehav.2012.12.024
Purcell S, Neale B, Todd-Brown K, Thomas L et al (2007) Plink: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. https://doi.org/10.1086/519795
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Reboreda JC, Clayton NS, Kacelnik A (1996) Species and sex differences in hippocampus size in parasitic and nonparasitic cowbirds. NeuroReport 7:505–508. https://doi.org/10.1097/00001756-199601310-00031
Rochette N, Rivera-Colón A, Catchen J (2019) Stacks 2: analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol 28:4737–4754. https://doi.org/10.1111/mec.15253
Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst 21:481–508
Rutila J, Latja R, Koskela K (2002) The common cuckoo Cuculus canorus and its cavity nesting hosts, 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
Sato NJ, Mikami OK, Ueda K (2010) The egg dilution effect hypothesis: a condition under which parasitic nestling ejection behaviour will evolve. Ornithol Sci 9:115–121. https://doi.org/10.2326/osj.9.115
Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113. https://doi.org/10.1111/j.2041-210X.2010.00012.x
Seel DC (1973) Egg-Laying by the Cuckoo Brit Birds 66:528–535
Soler M, Soler JJ, Martínez JG, Møller AP (1994) Micro-evolutionary change in host response to a brood parasite. Behav Ecol Sociobiol 35:295–301. https://doi.org/10.1007/BF00170710
Soler M, Palomino JJ, Martínez JG, Soler JJ (1995) Communal parental care by monogamous magpie hosts of fledgling great spotted cuckoos. Condor 97:804–810
Soler M, Soler JJ, Martínez JG (1998) Duration of sympatry and coevolution between the great spotted cuckoo (Clamator glandarius) and its primary host, the magpie (Pica pica). In: Rothstein SI, Robinson S (eds) Parasitic birds and their hosts: studies on coevolution. Oxford University Press, New York, pp 113–142
Spottiswoode CN (2013) A brood parasite selects for its own egg traits. Biol Lett 9:20130573. https://doi.org/10.1098/rsbl.2013.0573
Šulc M, Procházka P, Čapek M, Honza M (2016) Common cuckoo females are not choosy when removing an egg during parasitism. Behav Ecol 27:1642–1649. https://doi.org/10.1093/beheco/arw085
Šulc M, Troscianko J, Štětková G, Hughes AE, Jelínek V, Čapek M, Honza M (2019) Mimicry cannot explain rejection type in a host-brood parasite system. Anim Behav 155:111–118. https://doi.org/10.1016/j.anbehav.2019.05.021
Šulc M, Hughes AE, Troscianko J, Štětková G, Procházka P, Požgayová M, Piálek L, Piálková R, Brlík V, Honza M (2021) Automatic identification of bird females using egg phenotype. Zool J Linn Soc-Lond 195:33–44. https://doi.org/10.1093/zoolinnean/zlab051
Trine CL (2000) Effects of multiple parasitism on cowbird and wood thrush nesting success. In: Smith JNM, Cook TL, Rothstein SI, Robinson SK, Sealy SG (eds) Ecology and management of cowbirds. University of Texas Press, Austin, pp 135–144
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
Troscianko J, Stevens M (2015) Image calibration and analysis toolbox–a free software suite for objectively measuring reflectance, colour and pattern. Methods Ecol Evol 6:1320–1331. https://doi.org/10.1111/2041-210X.12439
Tuero DT, Fiorini VD, Reboreda JC (2007) Effects of shiny cowbird Molothrus bonariensis parasitism on different components of house wren Troglodytes aedon reproductive success. Ibis 149:521–529. https://doi.org/10.1111/j.1474-919X.2007.00676.x
Ursino CA, Strong MJ, Reboreda JC, Riehl C (2020) Genetic patterns of repeat and multiple parasitism by screaming cowbirds, a specialist brood parasite. Anim Behav 167:177–183. https://doi.org/10.1016/j.anbehav.2020.07.012
van den Berg CP, Troscianko J, Endler JA, Marshall NJ, Cheney KL (2020) Quantitative colour pattern analysis (QCPA): a comprehensive framework for the analysis of colour patterns in nature. Methods Ecol Evol 11:316–332. https://doi.org/10.1111/2041-210X.13328
Wyllie I (1975) Study of cuckoos and reed warblers. Brit Birds 68:369–378
Wyllie I (1981) The cuckoo. Batsford, London
Yang C, Stokke BG, Antonov A, Cai Y, Shi S, Moksnes A, Røskaft E, Møller AP, Liang W, Grim T (2013) Host selection in parasitic birds: are open-cup nesting insectivorous passerines always suitable cuckoo hosts? J Avian Biol 44:216–220. https://doi.org/10.1111/j.1600-048X.2013.00123.x
Yang CC, Li DL, Wang LW, Liang GX, Zhang ZW, Liang W (2014) Geographic variation in parasitism rates of two sympatric cuckoo hosts in China. Zool Res 35:67–71. https://doi.org/10.11813/j.issn.0254-5853.2014.1.067
Zölei A, Bán M, Moskát C (2015) No change in common cuckoo Cuculus canorus parasitism and great reed warblers’ Acrocephalus arundinaceus egg rejection after seven decades. J Avian Biol 46:570–576. https://doi.org/10.1111/jav.00673
Acknowledgements
We would like to thank Vojtěch Brlík, Miroslav Čapek, Terézia Mikolášová, Kateřina Sosnovcová, and Radka Valterová for their invaluable help in the field. We also thank Lisandrina Mari for her advice on graphical outputs and Vladimír Beneš and the European Molecular Biology Laboratory Genomic Core Facility in Heidelberg (Germany) for their kind advice and technical support regarding Illumina sequencing. Finally, we are grateful to the managers of the Hodonín Fish Farm for permission to conduct the fieldwork on their grounds and to Manuel Soler and two anonymous reviewers for their constructive comments.
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This work was supported by the Czech Science Foundation (grant no. 22-26812S provided to MH). JK was also supported by the Charles University Research Centre program no. 204069. Computational resources were supplied by the project “e-Infrastruktura CZ” (e-INFRA CZ LM2018140) supported by the Ministry of Education, Youth and Sports of the Czech Republic.
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MH, MŠ, MP, PP, GŠ, VJ, and JK contributed to the study conceptualization and field data collection; LP and RP conducted lab work and bioinformatics analyses; JK, AEH, and MŠ analysed the data statistically and prepared their visualization; MH acquired funding, and MH and JK wrote the first version of the manuscript. All authors commented on the first version and provided revisions of all drafts.
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Honza, M., Koleček, J., Piálek, L. et al. Multiple parasitism in an evictor brood parasite: patterns revealed by long-term monitoring, continuous video recording, and genetic analyses. Behav Ecol Sociobiol 76, 161 (2022). https://doi.org/10.1007/s00265-022-03270-x
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DOI: https://doi.org/10.1007/s00265-022-03270-x