Chinese Birds
Chinese Birds 2013, 4(1) 57-70 DOI:   10.5122/cbirds.2013.0003  ISSN: 1674-7674 CN: 11-5870/Q

Current Issue | Archive | Search                                                            [Print]   [Close]
ORIGINAL ARTICLE

Information and Service
This Article
Supporting info
PDF(412KB)
[HTML]
Reference
Service and feedback
Email this article to a colleague
Add to Bookshelf
Add to Citation Manager
Cite This Article
Email Alert
Keywords
brood parasitism
cowbirds
egg rejection
Molothrus
nest defense
Authors
Juan C. REBOREDA
Vanina D. FIORINI
María C. De MARSICO
PubMed
Article by Juan C. REBOREDA
Article by Vanina D. FIORINI
Article by María C. De MARSICO

Antiparasitic defenses in hosts of South American cowbirds

Juan C. REBOREDA *, Vanina D. FIORINI, María C. De MARSICO

Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires & IEGEBA-CONICET, Pabellón II Ciudad Universitaria, C1428EGA Buenos Aires, Argentina

Abstract

The cowbirds (Molothrus, Icteridae) are a monophyletic group that includes five extant brood-parasitic species. The Screaming (M. rufoaxillaris), Giant (M. oryzivorus) and Shiny (M. bonariensis) cowbirds range mostly in South America. Screaming and Shiny cowbirds are the ancestral and most recent species of the clade, respectively, therefore, differing in how long they have coevolved with their hosts. We present new experimental data on egg-rejection in a host of the Shiny Cowbird, the House Wren (Troglodytes aedon), review different lines of antiparasitic defenses in hosts of Screaming, Giant and Shiny cowbirds and assess whether hosts of different parasites differ in the type and extent of defenses. Hosts of all three parasites ejected non-mimetic eggs. Most hosts of Giant and Shiny cowbirds were grasp ejectors, whereas the main host of the Screaming Cowbird (the Baywing, Agelaioides badius) ejected parasitic eggs using its feet. Hosts smaller than Shiny Cowbirds neither ejected cowbird eggs nor deserted nests following parasitism. Some hosts also reacted more aggressively towards the parasite. The main host of Screaming Cowbird discriminated against non-mimetic chicks. Our results show that most hosts, regardless of the presumed evolutionary time of interaction with the parasite, have evolved some type of antiparasitic defense.

Keywords brood parasitism   cowbirds   egg rejection   Molothrus   nest defense  
Received 2012-12-16 Revised 2013-02-16 Online:  
DOI: 10.5122/cbirds.2013.0003
Corresponding Authors: Juan C. Reboreda
Email: reboreda@ege.fcen.uba.ar
About author:

References:
Antonov A, Stokke BG, Moksnes A, Røskaft E. 2009. Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host. Biol Lett, 5:169–171.
Astié AA, Reboreda JC. 2005. Creamy-bellied Thrush defences against Shiny Cowbird brood parasitism. Condor, 107:788–796.
Astié AA, Reboreda JC. 2006. Costs of egg punctures and Shiny Cowbird parasitism on Creamy-bellied Thrush reproductive success. Auk, 123:23–32.
Briskie JV, Sealy SG, Hobson KA. 1992. Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution, 46:334–340.
Budnik JM, Burhans DE, Ryan MR, Thompson FR. 2001. Nest desertion and apparent nest protection behavior by Bell’s Vireos in response to cowbird parasitism. Condor, 103:639–643.
Burhans DE, Strausberger BM, Carey MD. 2001. Regional variation in response of Field Sparrows to the threat of Brown-headed Cowbird parasitism. Auk, 118:776–780.
Clotfelter ED, Yasukawa K. 1999. Impact of brood parasitism by Brown-headed Cowbirds on Red-winged Blackbird reproductive success. Condor, 10:105–114.
Clotfelter ED. 1998. What cues do brown-headed cowbirds use to locate Red-winged Blackbird host nests? Anim Behav, 55:1181–1189.
Cruz A, Andrews RW. 1997. The breeding biology of the Pied Water-tyrant and its interactions with the Shiny Cowbird in Venezuela. J Field Ornithol, 68:91–97.
Cruz A, Manolis TD, Wiley JW. 1985. The Shiny Cowbird: A brood parasite expanding its range in the Caribbean region. Ornith Monogr, 36:607–620.
Cruz A, Prather JW, Post W, Wiley J. 1999. The spread of Shiny and Brown-headed Cowbirds into the Florida region. In: Smith JNM, Crook TL, Rothstein SI, Sealy SG Robinson SK (eds) Ecology and Management of Cowbirds. University of Texas Press, Austin, TX, pp 47–57.
Cruz A, Prather JW, Wiley JW, Weaver PF. 2008. Egg rejection behavior in a population exposed to parasitism: Village Weavers on Hispaniola. Behav Ecol, 19:398–403.
Cruz A, Wiley JW. 1989. The decline of an adaptation in the absence of a presumed selection pressure. Evolution, 43:55–62.
Cunningham EJA, Lewis S. 2006. Parasitism of maternal investment selects for increased clutch size and brood reduction in a host. Behav Ecol, 17:126–131.
Davies NB, Brooke MdeL, Kacelnik A. 1996. Recognition errors and probability of parasitism determine whether Reed Warblers should accept or reject mimetic cuckoo eggs. Proc R Soc B, 263:925–931.
Davies NB, Brooke MdeL. 1988. Cuckoos versus Reed Warblers: adaptations and counteradaptations. Anim Behav, 36:262–284.
Davies NB. 2000. Cuckoos, Cowbirds and Other Cheats. T. & A.D. Poyser, London.
Davies NB. 2011. Cuckoo adaptations: trickery and tuning. J Zool, 284:1–14.
Dawkins R, Krebs JR. 1979. Arms races between and within species. Proc R Soc B, 205:489–511.
de la Colina MA, Pompilio L, Hauber ME, Reboreda JC, Mahler B. 2012. Different recognition cues reveal the decision rules used for egg rejection by hosts of a variably mimetic avian brood parasite. Anim Cogn, 15:881–889.
De Mársico MC, Gantchoff MG, Reboreda JC. 2012. Host-parasite coevolution beyond the nestling stage? Mimicry of host fledglings by the specialist Screaming Cowbird. Proc R Soc B, 279:3401–3408.
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, in press.
De Mársico MC, Mahler B, Chomnalez M, Di Giacomo AG, Reboreda JC. 2010b. Host use by generalist and specialist brood parasitic cowbirds at population and individual levels. Adv Study Behav, 42:83–121.
De Mársico MC, Mahler B, Reboreda JC. 2010a. Reproductive success and nestling growth of Bay-winged Cowbirds parasitized by Screaming and Shiny cowbirds. Wilson J Ornithol, 122:417–431.
De Mársico MC, Reboreda JC. 2008a. Differential reproductive success favours strong host preferences in a highly specialized brood parasite. Proc R Soc B, 275:2499–2506.
De Mársico MC, Reboreda JC. 2008b. Egg-laying behaviour in Screaming Cowbirds. Why does a specialist brood parasite waste so many eggs? Condor, 110:143–153.
De Mársico MC, Reboreda JC. 2010. Brood parasitism increases mortality of Bay-winged Cowbird nests. Condor, 112:407–417.
Dearborn DC. 1999. Brown-headed Cowbird nestling vocalizations and risk of nest predation. Auk, 116:448–457.
Delhey K, Carrizo M, Verniere L, Mahler B, Peters A. 2011. Rejection of brood-parasitic Shiny Cowbird Molothrus bonariensis nestlings by the Firewood-gatherer Anumbius annumbi? J Avian Biol, 42:1–5.
Ellison K, Sealy SG. 2007. Small hosts infrequently disrupt laying by Brown-headed Cowbirds and Bronzed cowbirds. J Field Ornithol, 78:379–389.
Fiorini VD, Tuero DT, Reboreda JC. 2009a. Shiny Cowbirds benefits of synchronizing parasitism and puncturing eggs in large and small hosts. Anim Behav, 77:561–568.
Fiorini VD, Tuero DT, Reboreda JC. 2009b. Host behaviour and nest-site characteristics affect the likelihood of brood parasitism by Shiny Cowbirds on Chalk-browed Mockingbirds. Behaviour, 146:1387–1404.
Fraga RM. 1978. The Rufous-collared Sparrow as a host of the Shiny Cowbird. Wilson Bull, 90:271–284.
Fraga RM. 1980. The breeding of Rufous Horneros (Furnarius rufus). Condor, 82:58–68.
Fraga RM. 1985. Host-parasite interactions between Chalk-browed Mockingbirds and Shiny Cowbirds. Ornithol Monog, 36:829–844.
Fraga RM. 1998. Interactions of the parasitic screaming and Shiny Cowbirds (Molothrus rufoaxillaris and M. bonariensis) with a shared host, the Bay-winged Cowbird (M. badius). In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, Oxford, pp 173–193.
Fraga RM. 2011. Giant Cowbird (Molothrus oryzivorus) parasitism of Red-rumped Caciques (Cacicus haemorrhous) in the atlantic forest, northeastern Argentina. Wilson J Ornithol, 123: 277–282.
Friedmann H. 1929. The Cowbirds: A Study in the Biology of the Social Parasitism. C.C. Thomas, Springfield, IL.
Gill SA, Grieef PM, Staib LM, Sealy SG. 1997. Does nest defence deter or facilitate cowbird parasitism? A test of the nesting-cue hypothesis. Ethology, 103:56–71.
Gill SA, Sealy SG. 1996. Nest defence by Yellow Warblers: Recognition of a brood parasite and an avian nest predator. Behaviour, 133:263–282.
Gloag R, Fiorini VD, Reboreda JC, Kacelnik A. 2012. Brood parasite eggs enhance egg survivorship in a multiply parasitized host. Proc R Soc B, 279:1831–1839.
Goguen BG, Mathews NE. 1996. Nest desertion by Blue-gray Gnatcatchers in association with Brown-headed Cowbird parasitism. Anim Behav, 52:613–619.
Grim T, 2006. The evolution of nestling discrimination by hosts of parasitic birds: why is rejection so rare? Evol Ecol Res, 8:785–802.
Grim, T. 2007. Experimental evidence for chick discrimination without recognition in a brood parasite host. Proc R Soc B, 274:373–381.
Guigueno MF, Sealy SG. 2010. Clutch abandonment by parasitized Yellow Warblers: Egg burial or nest desertion? Condor, 112:399–406.
Guigueno MF, Sealy SG. 2011. Aggression towards egg-removing cowbird elicits clutch abandonment in parasitized Yellow Warblers, Dendroica petechia. Anim Behav, 81:211–218.
Hill DP, Sealy SG. 1994. Desertion of nest parasitized by cowbirds: have Clay-coloured Sparrow evolved an anti-parasite defense? Anim Behav, 48:1063–1070.
Hoover J, Robinson S. 2007. Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs. Proc Natl Acad Sci, USA, 104:4479–4483.
Hoover JP. 2003 Multiple effects of brood parasitism reduce the reproductive success of Prothonotary Warblers, Protonotaria citrea. Anim Behav, 65:923–934.
Hosoi SA, Rothstein SI. 2000. Nest desertion and cowbird parasitism: Evidence for evolved responses and evolutionary lag. Anim Behav, 59:823–840.
Kattan GH. 1998. Why do House Wrens accept Shiny Cowbird eggs? In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, Oxford, pp 212–220.
Kosciuch KL, Parker TH, Sandercock BK. 2006. Nest desertion by a cowbird host: an antiparasitic behavior or a response to egg loss? Behav Ecol, 17:917–924.
Krüger O. 2007. Cuckoos, cowbirds and hosts: adaptations, trade-offs and constraints. Phil Trans Roy Soc B, 362:1873–1886.
Krüger O. 2011. Brood parasitism selects for no defence in a cuckoo host. Proc R Soc B, 278:2777–2783.
Langmore NE, Hunt S, Kilner RM. 2003. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature, 422:157–160.
Lanyon SM. 1992. Interspecific brood parasitism in blackbirds (Icterinae): A phylogenetic perspective. Science, 255:77–79.
Lichtenstein G. 2001. Low success of shiny cowbird chicks parasitizing Rufous-bellied Thrushes: chick-chick competition or parental discrimination? Anim Behav, 61:401– 413.
Lorenzana JC, Sealy SG. 2001. Fitness costs and benefits of cowbird egg ejection by Gray Catbirds. Behav Ecol, 3:325–329.
Lotem A, Nakamura H, Zahavi A. 1992. Rejection of cuckoo eggs in relation to host age: A possible evolutionary equilibrium. Behav Ecol, 3:128–132.
Lotem A, Nakamura H, Zahavi A. 1995. Constraints on egg discrimination and cuckoo host coevolution. Anim Behav, 49:1185–1209.
Lowther PE. 2011. Lists of Victims and Hosts of the Parasitic Cowbirds (Molothrus). version: 02 Sep 2011. The Field Museum, Chicago, IL. http://fm1.fieldmuseum.org/aa/Files/lowther/CBList.pdf. Accessed 25 November 2012.
Mahler B, Lovette I, Confalonieri V, Reboreda JC. 2008. Eggshell spotting in brood parasitic Shiny Cowbirds (Molothrus bonariensis) is not linked to the female sex chromosome. Behav Ecol Sociobiol, 62:1193–1199.
Marchetti K. 1992. Costs to host defence and the persistence of parasitic cuckoos. Proc R Soc B, 248:41–45.
Mason P, Rothstein SI. 1986. Coevolution and avian brood parasitism-cowbird eggs show evolutionary response to host discrimination. Evolution, 40:1207–1214.
Mason P. 1986. Brood parasitism in a host generalist, the Shiny Cowbird: I. The quality of different species as hosts. Auk, 103:52–60.
Massoni V, Reboreda JC. 1998. Costs of parasitism and the lack of defenses on the Yellow-winged Blackbird-Shiny Cowbird system. Behav Ecol Sociobiol, 42:273–280.
Massoni V, Reboreda JC. 2002. A neglected cost of brood parasitism: egg punctures by Shiny Cowbirds during inspection of potential host nests. Condor, 104:407–412.
McLaren CM, Sealy SG. 2000. Are nest predation and brood parasitism correlated in Yellow Warblers? A test of the cowbird predation hypothesis. Auk, 117:1056–1060.
McMaster DG, Sealy SG.1999. Do Brown-headed Cowbird hatchlings alter adult Yellow Warbler behavior during the hatching period? J Field Ornithol, 70:365–373.
Mermoz ME, Fernández GJ. 1999. Low frequency of shiny cowbird parasitism on Scarlet-headed Blackbirds: Anti-parasite adaptations or nonspecific host life-history traits? J Avian Biol, 30:15–22.
Mermoz ME, Fernández GJ. 2003. Breeding success of a specialist brood parasite, the Screaming Cowbird, parasitizing an alternative host. Condor, 105:63–72.
Mermoz ME, Ornelas JF. 2004. Phylogenetic analysis of life-history adaptations in parasitic cowbirds. Behav Ecol 15:109–119.
Mermoz ME, Reboreda JC, Fernández GJ. Submitted. Are high rates of Shiny Cowbird parasitism in Brown-and-yellow Marshbirds consequence of lack of defenses? Submitted to Condor.
Moskát CT, Székely T, Cuthill IC, Kisbenedek T. 2008. Hosts’ responses to parasitic eggs: Which cues elicit hosts’ egg discrimination? Ethology, 114:186–194.
Neudorf DL, Sealy SG. 1994. Sunrise nest attentiveness in cowbird hosts. Condor, 96:162–169.
Ortega C. 1998. Cowbirds and Other Brood Parasites. The University of Arizona Press, Tucson.
Payne RB, Payne LL. 1998. Brood parasitism by cowbirds: risks and effects on reproductive success and survival in Indigo Buntings. Behav Ecol, 9:64–73.
Payne RB. 1977. The ecology of brood parasitism in birds. Ann Rev Ecol Syst, 8:1–28.
Peer BD, Ellison KS, Sealy SG. 2002. Intermediate frequencies of egg ejection by Northern Mockingbirds (Mimus polyglottos) sympatric with two cowbird species. Auk, 119:855–858.
Peer BD, Robinson SK, Herkert JR. 2000. Egg rejection by cowbird hosts in grasslands. Auk, 117:892–901.
Peer BD, Sealy SG. 2004. Correlates of egg rejection in hosts of the Brown-headed Cowbird. Condor, 106:580–599.
Picman J. 1989. Mechanism of increased puncture resistance of eggs of Brown-headed Cowbirds. Auk, 106:577–583.
Post W, Nakamura TK, Cruz, A. 1990. Patterns of Shiny Cowbird parasitism in St Lucia and southwestern Puerto Rico. Condor, 92:461–469.
Post W, Wiley JW. 1977a. The Shiny Cowbird in the West Indies. Condor, 79:119–121.
Post W, Wiley JW. 1977b. Reproductive interactions of Shiny Cowbird and Yellow-shouldered Blackbird. Condor, 79:176–184.
Rahn H, Curran-Everett L, Booth DT. 1988. Eggshell differences between parasitic and nonparasitic Icteridae. Condor, 90:962–964.
Rasmussen JL, Sealy SG, Underwood TJ. 2009. Video recording reveals the method of ejection of Brown-headed Cowbird eggs and no cost in American Robins and Gray Catbirds. Condor, 111:570–574.
Rasmussen JL, Sealy SG. 2006. Hosts feeding only Brown-headed Cowbird fledglings: where are the host fledglings? J Field Ornithol, 77:269–279.
Robert M, Sorci G. 1999. Rapid increase of host defence against brood parasites in a recently parasitized area: The case of Village Weavers in Hispaniola. Proc R Soc B, 266:941–946.
Robertson RJ, Norman RF. 1976. Behavioural defenses to brood parasitism by potencial hosts of the Brown-headed Cowbird. Condor, 78:166–173.
Robertson RJ, Norman RF. 1977. The function and evolution of aggressive host behaviour towards Brown-headed Cowbird (Molothrus ater). Can J Zool, 55:508–518.
Robinson SK. 1988. Foraging ecology and host relationships of Giant Cowbirds in southeastern Peru. Wilson Bull, 100:224–235.
Rohwer S, Spaw CD, Røskaft E. 1989. Costs to Northern Orioles of puncture-ejecting parasitic cowbird eggs from their nests. Auk, 106:734–738.
Rohwer S, Spaw CD. 1988. Evolutionary lag versus bill-size constraints: a comparative study of the acceptance of cowbird eggs by old hosts. Evol Ecol, 2:27–36.
Røskaft E, Moksnes A, Stokke BA, Bicik V, Moskát C. 2002. Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour, 139:613–628.
Røskaft E, Rohwer S, Spaw CD. 1993. Cost of puncture ejection compared with costs of rearing cowbird chicks for Northern Orioles. Ornis Scand, 24:28–32.
Rothstein SI, Patten MA, Fleischer RC. 2002. Phylogeny, specialization, and brood parasite-host coevolution: some possible pitfalls of parsimony. Behav Ecol, 13:1–10.
Rothstein SI. 1975. An experimental and teleonomic investigation of avian brood parasitism. Condor, 77:250–271.
Rothstein SI. 1977. Cowbird parasitism and egg recognition of Northern Oriole. Wilson Bull, 89:21–32.
Rothstein SI. 1990. A model system for coevolution: avian brood parasitism. Ann Rev Ecol Syst, 21:481–508.
Rothstein, SI, Robinson SK. 1998. The evolution and ecology of avian brood parasitism. In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, Oxford, pp 3–56.
Sackmann P, Reboreda JC. 2003. A comparative study of Shiny Cowbird parasitism in two large hosts: Chalk-browed Mockingbird and Rufous-bellied Thrush. Condor, 105:728–736.
Sato NJ, Mikami OK, Ueda K. 2010b. The egg dilution effect hypothesis: a condition under which parasitic nestling ejection behaviour will evolve. Ornithol Sci, 9:115–121.
Sato NJ, Tokue K, Noske RA, Mikami OK, Ueda K. 2010a. Evicting cuckoo nestlings from the nest: a new anti-parasitism behaviour. Biol Lett, 6:67–69.
Sealy SG, Neudorf DL, Hobson KE, Gill SA. 1998. Nest defense by potential hosts of the brown-headed cowbird: methodological approaches, benefits of defense and coevolution. In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, Oxford, pp 194–211.
Sealy SG. 1992. Removal of yellow warbler eggs in association with cowbird parasitism. Condor, 94:40–54.
Sealy SG. 1995. Burial of cowbird egg by parasitized yellow warblers: an empirical and experimental study. Anim Behav, 49:877–889.
Segura LN, Reboreda JC. 2012. Red-crested Cardinal defenses against Shiny Cowbird parasitism. Behaviour, 149:325–343.
Smith JNM, Arcese P, McLean IG. 1984. Age, experience and enemy recognition by wild Song Sparrows. Behav Ecol Sociobiol, 14:101–106.
Smith JNM, Taitt MJ, Zanette L, Myers-Smith IH. 2003. How do Brown-headed Cowbirds (Molothrus ater) cause nest failures in Song Sparrows (Melospiza melodia)? A removal experiment. Auk, 120:772–783.
Smith NG. 1968. The advantage of being parasitized. Nature, 219:690–694.
Soler M, Møller AP. 1990. Duration of sympatry and coevolution between the Great Spotted Cuckoo and its magpie host. Nature, 343:748–750.
Sorenson MD, Payne RB. 2002. Molecular genetic perspectives on avian brood parasitism. Integr Comp Biol, 42:388–400.
Spaw CD, Rowher S. 1987. A comparative study of eggshell thickness in cowbird and other passerines. Condor, 89:307–318.
Tokue K, Ueda K. 2010. Mangrove gerygones Gerygones laevigaster eject Little Bronze-cuckoo Chalcites minutillus hatchlings from parasitized nests. Ibis, 152: 835–839.
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 and Their Hosts. University of Texas Press, Austin, Texas, USA, pp 135–144.
Tuero DT, Fiorini VD, Reboreda JC. 2007. Effects of Shiny Cowbird parasitism on different components of House Wren reproductive success. Ibis, 149:521–527.
Underwood TJ, Sealy SG. 2006. Grasp-ejection in two small ejecters of cowbird eggs: a test of bill-size constraints and the evolutionary equilibrium hypothesis. Anim Behav, 71:409–416.
Uyehara JC, Narins PM. 1995. Nest defense by Willow Flycatchers to brood-parasitic intruders. Condor, 97:361–368.
Webster MS. 1994. Interspecific brood parasitism of Montezuma Oropendolas by Giant Cowbirds: parasitism or mutualism? Condor, 96:794–798.
Similar articles

Copyright by Chinese Birds