Adaptaciones y contraadaptaciones entre el Tordo Pico Corto (Molothrus rufoaxillaris) y el Tordo Músico (Agelaioides badius)

María Cecilia De Mársico; Juan Carlos Reboreda

doi:10.56178/eh.v29i1.619

Points of View Published 01 August 2014 https://doi.org/10.56178/eh.v29i1.619

Adaptations and counteradaptations between the Screaming Cowbird (Molothrus rufoaxillaris) and the Baywing (Agelaioides badius)

Agelaioides badius brood parasitism coevolution mimicry Molothrus

María Cecilia De Mársico Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Pabellón 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina | IEGEBA (UBA–CONICET). Pabellón 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina

Juan Carlos Reboreda Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Pabellón 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina | IEGEBA (UBA–CONICET). Pabellón 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina

Abstract

Avian obligate brood parasites exploit the parental care of individuals of other species (hosts) that rear the parasitic offspring at the expense of their own reproductive success. The costs of parasitism select for antiparasitic defences in host populations (i.e., adaptations that reduce the impact of parasitism). This, in turn, may favour counteradaptations in the parasite population, leading to a coevolutionary arms race between parasite and host. We review the reciprocal adaptations between a specialist brood parasite, the Screaming Cowbird (Molothrus rufoaxillaris), and its primary host, the Baywing (Agelaioides badius). The defences of the Baywing include the rejection of parasitic females, a little predictable egg-laying behaviour, the rejection of whole “superparasitized” clutches, and discrimination against juveniles that do not resemble their own. These defences are partially countered by the Screaming Cowbird through an elusive behaviour and rapid egg-laying, a close monitoring of host nesting activities and the evolution of visual and vocal mimicry of host young in the parasite juveniles. These results suggest an escalated arms race between the Screaming Cowbird and the Baywing through the entire nesting cycle. Future studies of the interactions between these species before, during and after parasitism might improve the understanding of host-parasite coevolutionary processes and the evolution of specialization in host use in brood parasitic birds.

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References

BRISKIE JV Y SEALY SG (1989) Changes in nest defenseagainst a brood parasite over the breeding cycle.Ethology 82:61–67
BROOKE ML Y DAVIES NB (1988) Egg mimicry by cuck-oos Cuculus canorus in relation to discrimination byhosts. Nature 335:630–632
BROOKER MG Y BROOKER LC (1991) Eggshell strengthin cuckoos and cowbirds. Ibis 133:406–413
BURHANS DE (1997) Habitat and microhabitat featuresassociated with cowbird parasitism in two forestedge cowbird hosts. Condor 99:866–872
CLOTFELTER ED (1998) What cues do brown-headedcowbirds use to locate red-winged blackbird hostnests? Animal Behaviour 55:1181–1189
DAVIES NB (2000) Cuckoos, cowbirds and other cheats.A&T Poyser, Londres
DAVIES NB Y BROOKE ML (1988) Cuckoos versus reedwarblers: adaptations and counteradaptations. Ani-mal Behaviour 36:262–284
DAVIES NB, BROOKE ML Y KACELNIK A (1996) Recogni-tion errors and probability of parasitism determinewhether reed warblers should accept or rejectmimetic cuckoo eggs. Proceedings of the Royal SocietyB 263:925–931
DAWKINS R Y KREBS JR (1979) Arms races between andwithin species. Proceedings of the Royal Society B205:489–511
DEARBORN DC, ANDERS A, THOMPSON FR III Y FAABORGJ (1998) Effects of cowbird parasitism on parentalprovisioning and nestling food acquisition andgrowth. Condor 100:326–334
DE MÁRSICO MC, GANTCHOFF MG Y REBOREDA JC(2012) Host-parasite coevolution beyond the nes-tling stage? Mimicry of host fledglings by the spe-cialist screaming cowbird. Proceedings of the RoyalSociety B 279:3401–3408
DE MÁRSICO MC, GLOAG R, URSINO CA Y REBOREDA JC(2013) A novel method of rejection of brood para-sitic eggs reduces parasitism intensity in a cowbirdhost. Biology Letters 9:20130076
DE MÁRSICO MC, MAHLER B Y REBOREDA JC (2010)Reproductive success and nestling growth of theBaywing parasitized by Screaming and ShinyCowbirds. Wilson Journal of Ornithology 122:417–431
DE MÁRSICO MC Y REBOREDA JC (2008a) Differentialreproductive success favours strong host preferencein a highly specialized brood parasite. Proceedingsof the Royal Society B 275:2499–2506
DE MÁRSICO MC Y REBOREDA JC (2008b) Egg-layingbehavior in screaming cowbirds: why does a spe-cialist brood parasite waste so many eggs? Condor110:143–153
DE MÁRSICO MC Y REBOREDA JC (2010) Brood parasit-ism increases mortality of Bay-winged cowbirdnests. Condor 112:407–417
DI GIACOMO AG Y REBOREDA JC (en prensa) Repro-ductive success of the specialist brood parasiteScreaming Cowbird in an alternative host, theChopi Blackbird. Auk
FEENEY WE, WELBERGEN JA Y LANGMORE NE (2012) Thefrontline of avian brood parasite–host coevolu-tion. Animal Behaviour 84:3–12
FRAGA RM (1991) The social system of a communalbreeder, the Bay-winged Cowbird Molothrus badius.Ethology 89:195–210
FRAGA RM (1996) Further evidence of parasitism ofChopi Blackbirds (Gnorimopsar chopi) by the special-ized Screaming Cowbird (Molothrus rufoaxillaris).Condor 98:866–867
FRAGA RM (1998) Interactions of the parasitic Scream-ing and Shiny Cowbirds (Molothrus rufoaxillaris andM. bonariensis) with a shared host, the Bay-wingedCowbird (M. badius). Pp. 173–193 en: ROBINSON SKY ROTHSTEIN SI (eds) Brood parasites and their hosts.Studies in coevolution. Oxford University Press,Nueva York
GIBBS HL, SORENSON MD, MARCHETTI K, BROOKE ML,DAVIES NB Y NAKAMURA H (2000) Genetic evidencefor female host-specific races of the commoncuckoo. Nature 407:183–186
GLOAG R, FIORINI V, REBOREDA JC Y KACELNIK A (2012)Brood parasite eggs enhance egg survivorship in amultiply parasitized host. Proceedings of the RoyalSociety B 279:1831–1839
GLOAG R, FIORINI V, REBOREDA JC Y KACELNIK A (2013)The wages of violence: mobbing by mockingbirdsas a frontline defence against brood-parasiticcowbirds. Animal Behaviour 86:1023–1029
GRIM T (2006) The evolution of nestling discrimina-tion by hosts of parasitic birds: why is rejection sorare? Evolutionary Ecology Research 8:785–802
HÖY G Y OTTOW J (1964) Biological and oological stud-ies of the Molothrine cowbirds (Icteridae) of Argen-tina. Auk 81:186–203
HUDSON WH (1874) Notes on the procreant instinctsof the three species of Molothrus found in BuenosAyres. Proceedings of the Zoological Society of London42:153–174
LANGMORE NE, FEENEY WE, CROWE-RIDDELL J, LUANH, LOUWRENS KM Y COCKBURN A (2012) Learned re-cognition of brood parasitic cuckoos in the superb fairy-wren Malurus cyaneus. Behavioral Ecology 23:798–805
LANGMORE NE, HUNT S Y KILNER RM (2003) Escalationof a coevolutionary arms race through host rejec-tion of brood parasitic young. Nature 422:157–160
LANGMORE NE, STEVENS M, MAURER G, HEINSOHN R,HALL ML, PETERS A Y KILNER RM (2011) Visual mim-icry of host nestlings by cuckoos. Proceedings of theRoyal Society B 278:2455–2463
LANYON SM (1992) Interspecific brood parasitism inblackbirds (Icterinae): a phylogenetic perspective.Science 225:77–79
LOTEM A (1993) Learning to recognize nestlings ismaladaptive for cuckoo Cuculus canorus hosts.Nature 362:743–745
LOTEM A, NAKAMURA H Y ZAHAVI A (1995) Constraintson egg discrimination and cuckoo–host co-evolution. Animal Behaviour 49:1185–1209
MARCHETTI K, NAKAMURA H Y GIBBS HL (1998) Host raceformation in the common cuckoo. Science 282:471–782
MASON P (1980) Ecological and evolutionary aspects ofhost selection in cowbirds. Tesis doctoral, Universityof Texas, Austin
MASON P (1987) Pair formation in cowbirds: evidencefound for Screaming but not Shiny cowbirds.Condor 89:349–356
MERMOZ ME Y FERNÁNDEZ GJ (2003) Breeding successof a specialist brood parasite, the screaming cowbird,parasitizing an alternative host. Condor 105:63–72
MERMOZ ME Y ORNELAS JF (2004) Phylogenetic analy-sis of life-history adaptations in parasitic cowbirds.Behavioral Ecology 15:109–119
MERMOZ ME Y REBOREDA JC (1996) New host for aspecialized brood parasite, the screaming cowbird.Condor 98:630–632
MOSKÁT C Y HONZA M (2000) Effect of nest and nestsite characteristics on the risk of cuckoo Cuculuscanorus parasitism in the great reed warblerAcrocephalus arundinaceus. Ecography 23:335–341
PEER BD (2006) Egg destruction and egg removal byavian brood parasites: adaptiveness and conse-quences. Auk 123:16–22
PICMAN J (1989) Mechanisms of increased punctureresistance of eggs of Brown-headed Cowbirds. Auk106:577–583
ROBERTSON RJ Y NORMAN RF (1977) The function andevolution of aggressive host behavior towards theBrown-headed Cowbird (Molothrus ater). CanadianJournal of Zoology 55:508–518
ROTHSTEIN SI (1975) Evolutionary rates and hostdefenses against avian brood parasitism. AmericanNaturalist 109:161–176
ROTHSTEIN SI (1990) A model system for coevolution:avian brood parasitism. Annual Review of Ecology andSystematics 21:481–508
ROTHSTEIN SI Y ROBINSON SK (1998) The evolution andecology of avian brood parasitism. An overview.Pp. 3–56 en: ROBINSON SK Y ROTHSTEIN SI (eds) Broodparasites and their hosts. Studies in coevolution. OxfordUniversity Press, Nueva York
SAT O NJ, TOKUE K, NOSKE RA, MIKAMI OK Y UEDA K(2009) Evicting cuckoo nestlings from the nest: anew anti-parasitism behaviour. Biology Letters6:67–69
SCARDAMAGLIA RC Y REBOREDA JC (2014) Rangingbehavior of female and male Shiny Cowbirds andScreaming Cowbirds while searching for host nests.Auk 131:610–618
SEALY SG (1992) Removal of Yellow Warbler eggs inassociation with cowbird parasitism. Condor94:40–54
SPAW CD Y ROHWER S (1987) A comparative study ofeggshell thickness in cowbirds and other passerines.Condor 89:307–318S
POTTISWOODE CN Y COLEBROOK-ROBJENT JFR (2007)Egg puncturing by the brood parasitic GreaterHoneyguide and potential host counteradaptations.Behavioral Ecology 18:792–799
SPOTTISWOODE CN Y KOOREVAAR J (2012) A stab in thedark: chick killing by brood parasitic honeyguides.Biology Letters 8:241–244
SPOTTISWOODE CN, STRYJEWSKI KF, QUADER S, COLE-BROOK-ROBJENT JF Y SORENSON MD (2011) Ancienthost specificity within a single species of brood para-sitic bird. Proceedings of the National Academy of Sci-ences 108:17738–17742
THOROGOOD R Y DAVIES NB (2013) Hawk mimicry andthe evolution of polymorphic cuckoos. ChineseBirds 4:39–50
TOKUE K Y UEDA K (2010) Mangrove GerygonesGerygone laevigaster eject Little Bronze-cuckooChalcites minutillus hatchlings from parasitizednests. Ibis 152:835–839
TRNKA A Y PROKOP P (2012) The effectiveness of hawkmimicry in protecting cuckoos from aggressivehosts. Animal Behaviour 83:263–268
URSINO CA, DE MÁRSICO MC, SUED M, FARALL A YREBOREDA JC (2011) Brood parasitism disproportion-ately increases nest provisioning and helper recruit-ment in a cooperatively breeding bird. BehavioralEcology and Sociobiology 65:2279–2286
WELBERGEN JA Y DAVIES NB (2011) A parasite in wolf ’sclothing: hawk mimicry reduces mobbing ofcuckoos by hosts. Behavioral Ecology 22:574–579

How to cite

María Cecilia De Mársico, Juan Carlos Reboreda (2014). Adaptations and counteradaptations between the Screaming Cowbird (Molothrus rufoaxillaris) and the Baywing (Agelaioides badius). El Hornero, Vol. 29 No. 1 (2014), 1-12. https://doi.org/10.56178/eh.v29i1.619

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[1] BRISKIE JV Y SEALY SG (1989) Changes in nest defenseagainst a brood parasite over the breeding cycle.Ethology 82:61–67

[2] BROOKE ML Y DAVIES NB (1988) Egg mimicry by cuck-oos Cuculus canorus in relation to discrimination byhosts. Nature 335:630–632

[3] BROOKER MG Y BROOKER LC (1991) Eggshell strengthin cuckoos and cowbirds. Ibis 133:406–413

[4] BURHANS DE (1997) Habitat and microhabitat featuresassociated with cowbird parasitism in two forestedge cowbird hosts. Condor 99:866–872

[5] CLOTFELTER ED (1998) What cues do brown-headedcowbirds use to locate red-winged blackbird hostnests? Animal Behaviour 55:1181–1189

[6] DAVIES NB (2000) Cuckoos, cowbirds and other cheats.A&T Poyser, Londres

[7] DAVIES NB Y BROOKE ML (1988) Cuckoos versus reedwarblers: adaptations and counteradaptations. Ani-mal Behaviour 36:262–284

[8] DAVIES NB, BROOKE ML Y KACELNIK A (1996) Recogni-tion errors and probability of parasitism determinewhether reed warblers should accept or rejectmimetic cuckoo eggs. Proceedings of the Royal SocietyB 263:925–931

[9] DAWKINS R Y KREBS JR (1979) Arms races between andwithin species. Proceedings of the Royal Society B205:489–511

[10] DEARBORN DC, ANDERS A, THOMPSON FR III Y FAABORGJ (1998) Effects of cowbird parasitism on parentalprovisioning and nestling food acquisition andgrowth. Condor 100:326–334

[11] DE MÁRSICO MC, GANTCHOFF MG Y REBOREDA JC(2012) Host-parasite coevolution beyond the nes-tling stage? Mimicry of host fledglings by the spe-cialist screaming cowbird. Proceedings of the RoyalSociety B 279:3401–3408

[12] DE MÁRSICO MC, GLOAG R, URSINO CA Y REBOREDA JC(2013) A novel method of rejection of brood para-sitic eggs reduces parasitism intensity in a cowbirdhost. Biology Letters 9:20130076

[13] DE MÁRSICO MC, MAHLER B Y REBOREDA JC (2010)Reproductive success and nestling growth of theBaywing parasitized by Screaming and ShinyCowbirds. Wilson Journal of Ornithology 122:417–431

[14] DE MÁRSICO MC Y REBOREDA JC (2008a) Differentialreproductive success favours strong host preferencein a highly specialized brood parasite. Proceedingsof the Royal Society B 275:2499–2506

[15] DE MÁRSICO MC Y REBOREDA JC (2008b) Egg-layingbehavior in screaming cowbirds: why does a spe-cialist brood parasite waste so many eggs? Condor110:143–153

[16] DE MÁRSICO MC Y REBOREDA JC (2010) Brood parasit-ism increases mortality of Bay-winged cowbirdnests. Condor 112:407–417

[17] DI GIACOMO AG Y REBOREDA JC (en prensa) Repro-ductive success of the specialist brood parasiteScreaming Cowbird in an alternative host, theChopi Blackbird. Auk

[18] FEENEY WE, WELBERGEN JA Y LANGMORE NE (2012) Thefrontline of avian brood parasite–host coevolu-tion. Animal Behaviour 84:3–12

[19] FRAGA RM (1991) The social system of a communalbreeder, the Bay-winged Cowbird Molothrus badius.Ethology 89:195–210

[20] FRAGA RM (1996) Further evidence of parasitism ofChopi Blackbirds (Gnorimopsar chopi) by the special-ized Screaming Cowbird (Molothrus rufoaxillaris).Condor 98:866–867

[21] FRAGA RM (1998) Interactions of the parasitic Scream-ing and Shiny Cowbirds (Molothrus rufoaxillaris andM. bonariensis) with a shared host, the Bay-wingedCowbird (M. badius). Pp. 173–193 en: ROBINSON SKY ROTHSTEIN SI (eds) Brood parasites and their hosts.Studies in coevolution. Oxford University Press,Nueva York

[22] GIBBS HL, SORENSON MD, MARCHETTI K, BROOKE ML,DAVIES NB Y NAKAMURA H (2000) Genetic evidencefor female host-specific races of the commoncuckoo. Nature 407:183–186

[23] GLOAG R, FIORINI V, REBOREDA JC Y KACELNIK A (2012)Brood parasite eggs enhance egg survivorship in amultiply parasitized host. Proceedings of the RoyalSociety B 279:1831–1839

[24] GLOAG R, FIORINI V, REBOREDA JC Y KACELNIK A (2013)The wages of violence: mobbing by mockingbirdsas a frontline defence against brood-parasiticcowbirds. Animal Behaviour 86:1023–1029

[25] GRIM T (2006) The evolution of nestling discrimina-tion by hosts of parasitic birds: why is rejection sorare? Evolutionary Ecology Research 8:785–802

[26] HÖY G Y OTTOW J (1964) Biological and oological stud-ies of the Molothrine cowbirds (Icteridae) of Argen-tina. Auk 81:186–203

[27] HUDSON WH (1874) Notes on the procreant instinctsof the three species of Molothrus found in BuenosAyres. Proceedings of the Zoological Society of London42:153–174

[28] LANGMORE NE, FEENEY WE, CROWE-RIDDELL J, LUANH, LOUWRENS KM Y COCKBURN A (2012) Learned re-cognition of brood parasitic cuckoos in the superb fairy-wren Malurus cyaneus. Behavioral Ecology 23:798–805

[29] LANGMORE NE, HUNT S Y KILNER RM (2003) Escalationof a coevolutionary arms race through host rejec-tion of brood parasitic young. Nature 422:157–160

[30] LANGMORE NE, STEVENS M, MAURER G, HEINSOHN R,HALL ML, PETERS A Y KILNER RM (2011) Visual mim-icry of host nestlings by cuckoos. Proceedings of theRoyal Society B 278:2455–2463

[31] LANYON SM (1992) Interspecific brood parasitism inblackbirds (Icterinae): a phylogenetic perspective.Science 225:77–79

[32] LOTEM A (1993) Learning to recognize nestlings ismaladaptive for cuckoo Cuculus canorus hosts.Nature 362:743–745

[33] LOTEM A, NAKAMURA H Y ZAHAVI A (1995) Constraintson egg discrimination and cuckoo–host co-evolution. Animal Behaviour 49:1185–1209

[34] MARCHETTI K, NAKAMURA H Y GIBBS HL (1998) Host raceformation in the common cuckoo. Science 282:471–782

[35] MASON P (1980) Ecological and evolutionary aspects ofhost selection in cowbirds. Tesis doctoral, Universityof Texas, Austin

[36] MASON P (1987) Pair formation in cowbirds: evidencefound for Screaming but not Shiny cowbirds.Condor 89:349–356

[37] MERMOZ ME Y FERNÁNDEZ GJ (2003) Breeding successof a specialist brood parasite, the screaming cowbird,parasitizing an alternative host. Condor 105:63–72

[38] MERMOZ ME Y ORNELAS JF (2004) Phylogenetic analy-sis of life-history adaptations in parasitic cowbirds.Behavioral Ecology 15:109–119

[39] MERMOZ ME Y REBOREDA JC (1996) New host for aspecialized brood parasite, the screaming cowbird.Condor 98:630–632

[40] MOSKÁT C Y HONZA M (2000) Effect of nest and nestsite characteristics on the risk of cuckoo Cuculuscanorus parasitism in the great reed warblerAcrocephalus arundinaceus. Ecography 23:335–341

[41] PEER BD (2006) Egg destruction and egg removal byavian brood parasites: adaptiveness and conse-quences. Auk 123:16–22

[42] PICMAN J (1989) Mechanisms of increased punctureresistance of eggs of Brown-headed Cowbirds. Auk106:577–583

[43] ROBERTSON RJ Y NORMAN RF (1977) The function andevolution of aggressive host behavior towards theBrown-headed Cowbird (Molothrus ater). CanadianJournal of Zoology 55:508–518

[44] ROTHSTEIN SI (1975) Evolutionary rates and hostdefenses against avian brood parasitism. AmericanNaturalist 109:161–176

[45] ROTHSTEIN SI (1990) A model system for coevolution:avian brood parasitism. Annual Review of Ecology andSystematics 21:481–508

[46] ROTHSTEIN SI Y ROBINSON SK (1998) The evolution andecology of avian brood parasitism. An overview.Pp. 3–56 en: ROBINSON SK Y ROTHSTEIN SI (eds) Broodparasites and their hosts. Studies in coevolution. OxfordUniversity Press, Nueva York

[47] SAT O NJ, TOKUE K, NOSKE RA, MIKAMI OK Y UEDA K(2009) Evicting cuckoo nestlings from the nest: anew anti-parasitism behaviour. Biology Letters6:67–69

[48] SCARDAMAGLIA RC Y REBOREDA JC (2014) Rangingbehavior of female and male Shiny Cowbirds andScreaming Cowbirds while searching for host nests.Auk 131:610–618

[49] SEALY SG (1992) Removal of Yellow Warbler eggs inassociation with cowbird parasitism. Condor94:40–54

[50] SPAW CD Y ROHWER S (1987) A comparative study ofeggshell thickness in cowbirds and other passerines.Condor 89:307–318S

[51] POTTISWOODE CN Y COLEBROOK-ROBJENT JFR (2007)Egg puncturing by the brood parasitic GreaterHoneyguide and potential host counteradaptations.Behavioral Ecology 18:792–799

[52] SPOTTISWOODE CN Y KOOREVAAR J (2012) A stab in thedark: chick killing by brood parasitic honeyguides.Biology Letters 8:241–244

[53] SPOTTISWOODE CN, STRYJEWSKI KF, QUADER S, COLE-BROOK-ROBJENT JF Y SORENSON MD (2011) Ancienthost specificity within a single species of brood para-sitic bird. Proceedings of the National Academy of Sci-ences 108:17738–17742

[54] THOROGOOD R Y DAVIES NB (2013) Hawk mimicry andthe evolution of polymorphic cuckoos. ChineseBirds 4:39–50

[55] TOKUE K Y UEDA K (2010) Mangrove GerygonesGerygone laevigaster eject Little Bronze-cuckooChalcites minutillus hatchlings from parasitizednests. Ibis 152:835–839

[56] TRNKA A Y PROKOP P (2012) The effectiveness of hawkmimicry in protecting cuckoos from aggressivehosts. Animal Behaviour 83:263–268

[57] URSINO CA, DE MÁRSICO MC, SUED M, FARALL A YREBOREDA JC (2011) Brood parasitism disproportion-ately increases nest provisioning and helper recruit-ment in a cooperatively breeding bird. BehavioralEcology and Sociobiology 65:2279–2286

[58] WELBERGEN JA Y DAVIES NB (2011) A parasite in wolf ’sclothing: hawk mimicry reduces mobbing ofcuckoos by hosts. Behavioral Ecology 22:574–579