Parasites often manipulate host behaviors to achieve their own selfish fitness goals. However, the efficiency with which parasitic begging calls solicit foster parental care has not yet been compared across different avian obligate host-brood parasite systems. For example, the begging calls of nestmate-evictor parasites are predicted to solicit sufficient levels of foster parental provisioning for the sole parasitic chick in the nest, whereas the calls of nest-sharing parasites combine together with the begging by host nestmates to solicit provisions for the whole brood. We studied the red-winged blackbird (Agelaius phoeniceus), a host of the brood parasitic brown-headed cowbird (Molothrus ater), to test the effects of begging call playbacks of nestmate-evictor common cuckoos (Cuculus canorus) or nestmate-sharing cowbirds upon parental feeding patterns. As predicted, cuckoo calls elicited more parental feeding trips and the amount of food delivered than cowbird calls. Food provisioning to nestlings while hearing cuckoo begging calls was similar to that while hearing redwing calls, and both were higher relative to a control silence treatment, which suggested that the begging call acoustics of the cuckoo served as an efficient stimulus for parental care in this cuckoo-naïve host. The study also confirms that cowbird calls are not supernormal stimuli for parental provisions in this host species, as redwing begging calls themselves were similarly effective stimulants for conspecific parental provisioning behaviors. Future research should examine the acoustical bases and perceptual biases present in the cuckoo’s begging calls to efficiently solicit parental provisioning in both naïve and coevolved hosts.
Nestlings of different avian brood parasites use distinct strategies to survive and solicit parental provisions by heterospecific foster parents: some of them evict or otherwise kill host nestmate to grow up alone in the nest (e.g., common cuckoos), whereas others typically share the nest with host chicks (e.g., brown-headed cowbirds). However, the efficiency to solicit parental care through begging calls by brood parasitic young with respect to their nestmate-evictor versus nest-sharing strategies has not yet been evaluated. We focused on a cuckoo-naïve and cowbird-exposed host species, the red-winged blackbird, to compare the effects of begging call playbacks of parasites and conspecifics, relative to silence controls. We found that the begging calls of cuckoos, rather than the cowbirds, elicited more parental feeding in this cuckoo-naïve host. This implied that it was the nestmate-evictor strategy, rather than host familiarity, that improved the efficiency of the parasitic begging calls. Our results provide the first experimental data on the efficiency of begging calls between cuckoos and cowbirds within the same host species, and it contributes to our understanding of the divergent ontogenetic strategies of evolutionarily distinct avian brood parasites.
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Anderson MG, Brunton DH, Hauber ME (2010) Species-specificity of grey warbler begging solicitation and alarm calls revealed by nestling responses to playbacks. Anim Behav 79:401–409. https://doi.org/10.1016/j.anbehav.2009.11.017
Anderson MG, Moskat C, Ban M, Grim T, Cassey P, Hauber ME (2009) Egg eviction imposes a recoverable cost of virulence in chicks of a brood parasite. PLoS One 4:e7725. https://doi.org/10.1371/journal.pone.0007725
Anderson MG, Ross HA, Brunton DH, Hauber ME (2009) Begging call matching between a specialist brood parasite and its host: a comparative approach to detect coevolution. Biol J Linn Soc Lond 98:208–216. https://doi.org/10.1111/j.1095-8312.2009.01256.x
Bolopo D, Canestrari D, Roldán M, Baglione V, Soler M (2015) High begging intensity of great spotted cuckoo nestlings favours larger-size crow nest mates. Behav Ecol Sociobiol 69:873–882. https://doi.org/10.1007/s00265-015-1895-z
Bortolato T, Gloag R, Reboreda JC, Fiorini VD (2019) Size matters: shiny cowbirds secure more food than host nestmates thanks to their larger size, not signal exaggeration. Anim Behav 157:201–207. https://doi.org/10.1016/j.anbehav.2019.09.009
Brooke ML, Davies NB (1989) Provisioning of nestling cuckoos Cuculus canorus by reed warbler Acrocephalus scirpaceus hosts. Ibis 131:250–256. https://doi.org/10.1111/j.1474-919X.1989.tb02767.x
Burford J, Friedrich T, Yasukawa K (1998) Response to playback of nestling begging in the red-winged blackbird, Agelaius phoeniceus. Anim Behav 56:555–561. https://doi.org/10.1006/anbe.1998.0830
Clark AB, Lee WH (1998) Red-winged blackbird females fail to increase feeding in response to begging call playbacks. Anim Behav 56:563–570. https://doi.org/10.1006/anbe.1998.0831
Davies NB, Brooke ML (1988) Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav 36:262–284. https://doi.org/10.1016/S0003-3472(88)80269-0
Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205:489–511. https://doi.org/10.1098/rspb.1979.0081
Dearborn DC (1999) Brown-headed cowbird nestling vocalizations and the risk of nest predation. Auk 116:448–457. https://doi.org/10.2307/4089378
Dinets V, Samas P, Croston R, Grim T, Hauber ME (2015) Predicting the responses of native birds to trans-oceanic invasions by avian brood parasites. J Field Ornithol 86:244–251. https://doi.org/10.1111/jofo.12111
Dinets V, Sokolovskis K, Hanley D, Hauber ME (2018) Striking difference in response to expanding brood parasites by birds of western and eastern Beringia. J Field Ornithol 89:117–125. https://doi.org/10.1111/jofo.12247
Eastzer D, Chu PR, King AP (1980) The young cowbird: average or optimal nestling? Condor 82:417–425. https://doi.org/10.2307/1367567
Glassey B, Forbes S (2003) Why brown-headed cowbirds do not influence red-winged blackbird parent behavior. Anim Behav 65:1235–1246. https://doi.org/10.1006/anbe.2003.2168
Gloag R, Kacelnik A (2013) Host manipulation via begging call structure in the brood-parasitic shiny cowbird. Anim Behav 86:101–109. https://doi.org/10.1016/j.anbehav.2013.04.018
Gloag R, Tuero DT, Fiorini VD, Reboreda JC, Kacelnik A (2012) The economics of nestmate killing in avian brood parasites: a provisions trade-off. Behav Ecol 23:132–140. https://doi.org/10.1093/beheco/arr166
Grayson P, Glassey B, Forbes S (2013) Does brood parasitism induce paternal care in a polygynous host? Ethology 119:489–495. https://doi.org/10.1111/eth.12086
Grim T, Honza M (2001) Does supernormal stimulus influence parental behaviour of the cuckoo’s host? Behav Ecol Sociobiol 49:322–329. https://doi.org/10.1007/s002650000295
Hauber ME (2003a) Hatching asynchrony, nestling competition, and the cost of interspecific brood parasitism. Behav Ecol 14:224–235. https://doi.org/10.1093/beheco/14.2.227
Hauber ME (2003b) Lower begging responsiveness of host vs. cowbird nestlings is related to species identity but not to early social experience in parasitized broods. J Comp Psychol 117:24–30
Hauber ME, Moskát C (2008) Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts. Behav Ecol 19:79–86. https://doi.org/10.1093/beheco/arm108
Hauber ME, Ramsey CK (2003) Honesty in host-parasite communication signals: the case for begging by fledgling brown-headed cowbirds Molothrus ater. J Avian Biol 34:339–344. https://doi.org/10.1111/j.0908-8857.2003.03158.x
Holen ØH, Saetre GP, Slagsvold T, Stenseth NC (2001) Parasites and supernormal manipulation. Proc R Soc Lond B 268:2551–2558. https://doi.org/10.1098/rspb.2001.1818
Hoover JP, Reetz MJ (2006) Brood parasitism increases provisioning rate, and reduces offspring recruitment and adult return rates, in a cowbird host. Oecologia 149:165–173 https://www.jstor.org/stable/20445983
Jamie GA, Kilner RM (2017) Begging call mimicry by brood parasite nestlings: adaptation, manipulation and development. In: Soler M (ed) Avian brood parasitism: behaviour, ecology, evolution and coevolution. Springer Int. Publ, Cham, pp 517–538
Kilner R (2002) The evolution of complex begging displays. In: Wright J, Leonard ML (eds) The evolution of begging, competition, cooperation and communication. Kluwer, Dordrecht, pp 87–106
Kilner RM, Madden JR, Hauber ME (2004) Brood parasitic cowbird nestlings use host young to procure resources. Science 305:877–879. https://doi.org/10.1126/science.1098487
Kilner RM, Noble DG, Davies NB (1999) Signals of need in parent-offspring communication and their exploitation by the common cuckoo. Nature 397:667–672. https://doi.org/10.1038/17746
Kilpatrick AM (2002) Variation in growth of brown-headed cowbird (Molothrus ater) nestlings and energetic impacts on their host parents. Can J Zool 80:145–153. https://doi.org/10.1139/z01-217
Langmore NE, Hunt S, Kilner RM (2003) Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422:157–160. https://doi.org/10.1038/nature01460
Langmore NE, Maurer GJ, Kilner RM (2008) Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites basalis. Evolution 62:1689–1699. https://doi.org/10.1111/j.1558-5646.2008.00405.x
Lawson SL, Enos JK, Mendes NC, Gill SA, Hauber ME (2020) Heterospecific eavesdropping on an anti-parasitic referential alarm call. Commun Biol 3:143. https://doi.org/10.1038/s42003-020-0875-7
Li D, Li X, Zhang Y, Guan S, Ruan Y (2020) Contrasting effects of egg size and appearance on egg recognition and rejection response by Oriental reed warblers. Ecol Evol 10:10508-10519. https://doi.org/10.1002/ece3.6707
Li D, Zhang Z, Grim T, Liang W, Stokke BG (2016) Explaining variation in brood parasitism rates between potential host species with similar habitat requirements. Evol Ecol 30:905–923. https://doi.org/10.1007/s10682-016-9850-7
Lichtenstein G, Dearborn DC (2004) Begging and short-term need in cowbird nestlings: how different are brood parasites? Behav Ecol and Sociobiol 56:352–359. https://doi.org/10.1007/s00265-004-0795-4
Lichtenstein G, Sealy SG (1998) Nestling competition rather than supernormal stimulus, explains the success of parasitic brown-headed cowbirds in yellow warbler nests. Proc R Soc Lond B 265:249–254. https://doi.org/10.1098/rspb.1998.0289
Lorenzana JC, Sealy SG (1996) Are begging calls of generalist parasitic cowbirds adapted for brood parasitism? UFS (Delta Marsh) Annu Rep 31:85–93
Louder MIM, Lafayette M, Louder AA, Uy FMK, Balakrishnan CN, Yasukawa K, Hauber ME (2020) Shared transcriptional responses to con- and heterospecific behavioral antagonists in a wild songbird. Sci Rep 10:4092. https://doi.org/10.1038/s41598-020-60231-y
Madden JR, Davies NB (2006) A host-race difference in begging calls of nestling cuckoos Cuculus canorus develops through experience and increases host provisioning. Proc R Soc Lond B 273:2343–2351. https://doi.org/10.1098/rspb.2006.3585
Moskát C, Hauber ME, Louder MIM (2017) The evolution of nest sharing and nest mate killing strategies in brood parasites. In: Soler M (ed) Avian brood parasitism: behaviour, ecology, evolution and coevolution. Springer Int. Publ, Cham, pp 475–492
Ranjard L, Anderson M, Rayner M, Payne R, McLean I, Briskie J, Ross H, Brunton D, Woolley S, Hauber ME (2010) Bioacoustic distances between the begging calls of brood parasites and their host species: a comparison of metrics and techniques. Behav Ecol Sociobiol 64:1915–1926. https://doi.org/10.1007/s00265-010-1065-2
Rivers JW, Blundell MA, Loughin TM, Peer BD, Rothstein SI (2013) The exaggerated begging behaviour of an obligate brood parasite is shared with a nonparasitic close relative. Anim Behav 86:529–536. https://doi.org/10.1016/j.anbehav.2013.06.004
Rivers JW, Blundell MA, Rothstein SI (2014) Mismatched begging displays between foreign and host offspring reduce brood parasite fitness. Behav Ecol 25:785–793. https://doi.org/10.1093/beheco/aru055
Rivers JW, Loughin TM, Rothstein SI (2010) Brown-headed cowbird nestlings influence nestmate begging, but not parental feeding, in hosts of three distinct sizes. Anim Behav 79:107–116. https://doi.org/10.1016/j.anbehav.2009.10.009
Røskaft E, Orians GH, Beletsky LD (1990) Why do red-winged blackbirds accept eggs of brown-headed cowbirds? Evol Ecol 4:35–42. https://doi.org/10.1007/BF02270713
Rothstein SI (1975) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271. https://doi.org/10.2307/1366221
Schielzeth H, Dingemanse NJ, Nakagawa S, Westneat DF, Allegue H, Teplitsky C, Réale D, Dochtermann NA, Garamszegi LZ, Araya-Ajoy YG (2020) Robustness of linear mixed-effects models to violations of distributional assumptions. Methods Ecol Evol 11:1141–1152. https://doi.org/10.1111/2041-210X.13434
Slabbekoorn H, Peet M (2003) Birds sing at a higher pitch in urban noise. Nature 424:267. https://doi.org/10.1038/424267a
Soler M (2017) Begging behaviour, food delivery and food acquisition in nests with brood parasitic nestlings. In: Soler M (ed) Avian brood parasitism: behaviour, ecology, evolution and coevolution. Springer Int. Publ, Cham, pp 493–515
Soler M, Neve L, Roldán M, Macías-Sánchez E, Martín-Gálvez D (2012) Do great spotted cuckoo nestlings beg dishonestly? Anim Behav 83:163–169. https://doi.org/10.1016/j.anbehav.2011.10.022
Soler M, Soler JJ, Martinez JG, Møller AP (1995) Chick recognition and acceptance: a weakness in magpies exploited by the parasitic great spotted cuckoo. Behav Ecol Sociobiol 37:243–248. https://doi.org/10.1007/BF00177403
Tanaka KD, Ueda K (2005) Horsfield’s hawk-cuckoo nestlings simulate multiple gapes for begging. Science 308:653. https://doi.org/10.1126/science.1109957
Tinbergen N (1951) The study of instinct. Oxford University Press, Oxford
Weatherhead PJ (1989) Sex ratios, host-specific reproductive success, and impact of brown-headed cowbirds. Auk 106:358–366. https://doi.org/10.1093/auk/106.3.358
Weygoldt P (1980) Complex brood care and reproductive behaviour in captive poison-arrow frogs, Dendrobates pumilio O. Schmidt. Behav Ecol Sociobiol 7:329–332. https://doi.org/10.1007/BF00300674
Yang C, Wang L, Liang W, Møller AP (2015) Do common cuckoos (Cuculus canorus) possess an optimal laying behaviour to match their own egg phenotype to that of their Oriental reed warbler (Acrocephalus orientalis) hosts? Biol J Linn Soc 117:422–427. https://doi.org/10.1111/bij.12690
Yasukawa K, Berrios HK, Johannes AW (2016) A test of the nestling discrimination hypothesis for parasitism of red-winged blackbirds (Agelaius phoeniceus) by brown-headed cowbirds (Molothrus ater). Wilson J Ornithol 128:437–441. https://doi.org/10.1676/1559-4491-128.2.437
We thank Ken Yasukawa, Mikus Abolins-Abols, Matt Louder, and Alec Luro for their discussions during the experimental design. We would like to thank Thomas A. Gavin, Professor Emeritus, Cornell University, for his help with editing this paper. The editor and the referees of this journal gave constructive comments on draft manuscripts.
The study was funded partly by the National Geographic Society (NGS-60453R-19 to MEH) and the National Science Foundation (IOS #1953226 to MEH) and partly from the National Natural Science Foundation of China (Nos. 31911540468 and 31672316 to DL), the Natural Science Foundation of Liaoning Province of China (2019-MS-154 to DL), and the China Scholarship Council (No. 201806805010 to DL).
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and institutional guidelines for the use of animals were followed. This study was permitted by governmental (USFWS #MB08861A-3) and institutional (UIUC IACUC #17259) research agencies. No redwing nestling was harmed or died as a result of our manipulations, and we did not detect parents avoiding to feed during the experiment or any differences in predation rates between experimental and non-experimental nests.
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Li, D., Hauber, M.E. Parasitic begging calls of nestmate-evictor common cuckoos stimulate more parental provisions by red-winged blackbirds than calls of nest-sharing brown-headed cowbirds. Behav Ecol Sociobiol 75, 11 (2021). https://doi.org/10.1007/s00265-020-02955-5
- Begging calls
- Brood parasite
- Parental provisioning
- Supernormal stimulus