Abstract
Brown-headed cowbirds (Molothrus ater) deposit their eggs into the nests of other birds, which then raise the cowbird chick. Female cowbirds thus have limited options for impacting their offspring’s development via maternal effects compared to most other passerines. Cowbirds can impact their offspring’s phenotype by choosing among potential host nests, and by adjusting egg resources based on host characteristics. To examine whether cowbirds exhibit either or both of these strategies, we investigated rates of cowbird parasitism and egg investment (egg size, yolk-to-albumen ratio, and yolk testosterone and androstenedione) among and within host species in a shrubland bird community. We found that the probability of being parasitized by cowbirds, controlling for host status as a cowbird egg accepter or rejecter and ordinal date, varied significantly among host species, indicating an apparent preference for some hosts. Parasitism rates did not differ with host size, however, and despite variation in cowbird egg size among host species, this variation was not related to host size or cowbird preference. Among host species with eggs that are larger than those of the cowbird, cowbirds were significantly more likely to parasitize nests with relatively smaller eggs, whereas parasitism rates did not vary with relative egg size in host species with smaller eggs. There was no evidence for variation in cowbird egg components among or within host species. Our data indicate that cowbirds discriminate among host nests, but do not appear to adjust the composition of their eggs based on inter- or intraspecific host variation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alderson GW, Gibbs HL, Sealy SG (1999) Determining the reproductive behaviour of individual brown-headed cowbirds using microsatellite DNA markers. Anim Behav 58:895–905. doi:10.1006/anbe.1999.1220
Amundsen T, Lorentsen SH, Tveraa T (1996) Effects of egg size and parental quality on early nestling growth: an experiment with the Antarctic petrel. J Anim Ecol 65:545–555. doi:10.2307/5735
Amundsen T, Brobakken PT, Moksnes A, Røskaft E (2002) Rejection of common cuckoo Cuculus canorus eggs in relation to female age in the bluethroat Luscinia svecica. J Avian Biol 33:366–370. doi:10.1034/j.1600-048X.2002.02894.x
Ankney C, Johnson S (1985) Variation in weight and composition of brown-headed cowbird eggs. Condor 87:296–299. doi:10.2307/1366903
Badyaev AV, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc B-Biol Sci 364:1169–1177. doi:10.1098/rstb.2008.0302
Benson TJ, Brown JD, Bednarz JC (2010) Identifying predators clarifies predictors of nest success in a temperate passerine. J Anim Ecol 79:225–234. doi:10.1111/j.1365-2656.2009.01604.x
Blem CR (1990) Avian energy storage. Curr Ornithol 7:59–113
Briskie J, Sealy S, Hobson K (1990) Differential parasitism of least flycatchers and yellow warblers by the brown-headed cowbird. Behav Ecol Sociobiol 27:403–410. doi:10.1007/BF00164066
Carey C, Rahn H, Parisi P (1980) Calories, water, lipid and yolk in avian eggs. Condor 82:335–343. doi:10.2307/1367405
Chiavacci SJ (2016) Avian nest predation: relationships with landscape characteristics, and influences on nestling and adult behavior. Ph.D. Dissertation Department of Natural Resources, University of Illinois, Urbana-Champaign, IL
Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26. doi:10.1017/S1464793101005784
Clotfelter ED (1998) What cues do brown-headed cowbirds use to locate red-winged blackbird host nests? Anim Behav 55:1181–1189. doi:10.1006/anbe.1997.0638
Cunningham EJA, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77. doi:10.1038/35003565
Curson DR, Goguen CB, Mathews NE (2010) Community-level patterns of population recruitment in a generalist avian brood parasite, the brown-headed cowbird. Oecologia 163:601–612. doi:10.1007/s00442-010-1630-4
Eising CM, Groothuis TGG (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav 66:1027–1034. doi:10.1006/anbe.2003.2287
Fleischer R (1985) A new technique to identify and assess the dispersion of eggs of individual brood parasites. Behav Ecol Sociobiol 17:91–99
Fleischer R, Smyth A, Rothstein S (1987) Temporal and age-related variation in the laying rate of the parasitic brown-headed cowbird in the eastern Sierra-Nevada, California. Can J Zool-Rev Can Zool 65:2724–2730
Fontaine JJ, Martin TE (2006) Habitat selection responses of parents to offspring predation risk: an experimental test. Am Nat 168:811–818. doi:10.1086/508297
Freeman BM, Vince MA (1974) Development of the avian embryo: a behavioural and physiological study. Chapman and Hall, London
Friedmann H, Kiff FL (1985) The parasitic cowbirds and their hosts. Proc West Found Vert Zool 2:225–302
Goguen CB, Mathews NE (1996) Nest desertion by blue-gray gnatcatchers in association with brown-headed cowbird parasitism. Anim Behav 52:613–619. doi:10.1006/anbe.1996.0202
Grant ND, Sealy SG (2002) Selection of red-winged blackbird (Agelaius phoeniceus) hosts by the brown-headed cowbird (Molothrus ater). Bird Behav 15:21–30
Groothuis TGG, von Engelhardt N (2005) Investigating maternal hormones in avian eggs: measurement, manipulation, and interpretation. Ann New York Acad Sci 1046:168–180. doi:10.1196/annals.1343.014
Hahn DC, Smith G (2011) Life history trade-offs between longevity and immunity in the parasitic brown-headed cowbird. Open Evol J 5:8–13
Hahn DC, Hatfield JS, Abdelnabi MA et al (2005) Inter-species variation in yolk steroid levels and a cowbird-host comparison. J Avian Biol 36:40–46. doi:10.1111/j.0908-8857.2005.03040.x
Hahn DC, Sedgwick JA, Painter IS, Casna NJ (1999) A spatial and genetic analysis of cowbird host selection. Stud Avian Biol 18:204–217
Hauber ME (2003) Interspecific brood parasitism and the evolution of host clutch sizes. Evol Ecol Res 5:559–570
Hauber ME, Pilz KM (2003) Yolk testosterone levels are not consistently higher in the eggs of obligate brood parasites than their hosts. Am Midl Nat 149:354–362. doi:10.1674/0003-0031(2003)149[0354:YTLANC]2.0.CO;2
Holford K, Roby D (1993) Factors limiting fecundity of captive brown-headed cowbirds. Condor 95:536–545. doi:10.2307/1369597
Hoover JP, Robinson SK (2007) Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs. Proc Natl Acad Sci U S A 104:4479–4483. doi:10.1073/pnas.0609710104
Hosoi SA, Rothstein SI (2000) Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim Behav 59:823–840. doi:10.1006/anbe.1999.1370
Hoyt D (1979) Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73–77
Kattan GH (1997) Shiny cowbirds follow the “shotgun” strategy of brood parasitism. Anim Behav 53:647–654. doi:10.1006/anbe.1996.0339
Keys GC, Fleischer RC, Rothstein SI (1986) Relationships between elevation, reproduction and the hematocrit level of brown-headed cowbirds. Comp Biochem Physiol A Physiol 83:765–769. doi:10.1016/0300-9629(86)90725-5
Kilner RM, Madden JR, Hauber ME (2004) Brood parasitic cowbird nestlings use host young to procure resources. Science 305:877–879. doi:10.1126/science.1098487
King AP (1979) Variables affecting parasitism in the North American cowbird (Molothrus ater). Ph.D. Dissertation, Cornell University, Ithaca
Kozlovic DR, Knapton RW, Barlow JC (1996) Unsuitability of the House Finch as a host of the Brown-headed Cowbird. Condor 98:253–258. doi:10.2307/1369143
Kozlowski CP, Bauman JE, Hahn DC (2009) A simplified method for extracting androgens from avian egg yolks. Zoo Biol 28:137–143. doi:10.1002/zoo.20221
Krist M (2011) Egg size and offspring quality: a meta-analysis in birds. Biol Rev Camb Philos Soc 86:692–716. doi:10.1111/j.1469-185X.2010.00166.x
Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc Lond B 267:2005–2010. doi:10.1098/rspb.2000.1242
Littell RC, Milliken GA, Stroup WW, Wolfinger K, Schabenberger O (2006) SAS system for mixed models. SAS Institute Inc., Cary
Lotem A, Nakamura H, Zahavi A (1995) Constraints on egg discrimination and cuckoo-host co-evolution. Anim Behav 49:1185–1209. doi:10.1006/anbe.1995.0152
Mayfield H (1977) Brown-headed cowbird: Agent of extermination? Am Birds 31:107–113
Merrill L, O’Loghlen AL, Wingfield John C, Rothstein SI (2013) Immune function in an avian brood parasite and its nonparasitic relative. Physiol Biochem Zool 86:61–72. doi:10.1086/668852
Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Phil Trans R Soc B 363:1635–1645. doi:10.1098/rstb.2007.0011
Moskat C, Ban M, Hauber ME (2014) Naive hosts of avian brood parasites accept foreign eggs, whereas older hosts fine-tune foreign egg discrimination during laying. Front Zool 11:45. doi:10.1186/1742-9994-11-45
Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407. doi:10.1016/S0169-5347(98)01472-4
Nager RG (2006) The challenges of making eggs. Ardea 94:323–346
Newman AEM, Chin EH, Schmidt KL et al (2008) Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay. Gen Comp Endocrinol 155:503–510. doi:10.1016/j.ygcen.2007.08.007
Nolan V Jr (1978) The ecology and behavior of the Prairie Warbler, Dendroica discolor. Ornithological monograph No 26. American Ornithologists’ Union, Washington D.C
Norman R, Robertson R (1975) Nest-searching behavior in brown-headed cowbird. Auk 92:610–611
Ojanen M (1983) Composition of the eggs of the Great tit (Parus major) and the Pied flycatcher (Ficedula hypoleuca). Ann Zool Fenn 20:57–63
Ortega JC, Ortega CP (2009) Sex ratios and survival probabilities of brown-headed cowbirds (Molothrus ater) in southwest Colorado. Auk 126:268–277. doi:10.1525/auk.2009.07147
Ortega C, Ortega J, Cruz A (1994) Use of artificial brown-headed cowbird eggs as a potential management tool in deterring parasitism. J Wildl Manage 58:488–492. doi:10.2307/3809320
Parsons J (1970) Relationship between egg size and post-hatching chick mortality in herring gull (Larus argentatus). Nature 228:1221. doi:10.1038/2281221a0
Payne RB (1976) The clutch size and numbers of eggs of brown-headed cowbirds: effects of latitude and breeding season. Condor 78:337–342. doi:10.2307/1367693
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. doi:10.1093/beheco/9.1.64
Peer BD, Sealy SG (2004) Correlates of egg rejection in hosts of the Brown-headed Cowbird. Condor 106:580–599. doi:10.1650/7412
Poisbleau M, Carslake D, Demongin L et al (2011) Yolk androgen deposition without an energetic cost for female rockhopper penguins: a compensatory strategy to accelerate brood reduction? Biol Lett 7:605–607. doi:10.1098/rsbl.2010.1134
Procházka P, Konvičková-Patzenhauerová H, Požgayová M et al (2014) Host genotype and age have no effect on rejection of parasitic eggs. Naturwissenschaften 101:417–426. doi:10.1007/s00114-014-1171-5
Reid W, Boersma P (1990) Parental quality and selection on egg size in the magellanic penguin. Evolution 44:1780–1786. doi:10.2307/2409506
Rivers JW (2007) Nest mate size, but not short-term need, influences begging behavior of a generalist brood parasite. Behav Ecol 18:222–230. doi:10.1093/beheco/arl068
Rothstein SI (1975) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271. doi:10.2307/1366221
Rothstein SI (1976) Cowbird parasitism of cedar waxwing and its evolutionary implications. Auk 93:498–509
Rothstein SI (1978) Mechanisms of avian egg-recognition—additional evidence for learned components. Anim Behav 26:671. doi:10.1016/0003-3472(78)90133-1
Rothstein SI (1990) A model system for coevolution avian brood parasitism. In: Johnston RF (ed) Annual review of ecology and systematics, vol 21. Annual Reviews Inc.: Palo Alto, California, pp 481–508
Rothstein SI, Robinson SK (1998) The evolution and ecology of avian brood parasitism. Oxford University Press, New York
Royle NJ, Hall ME, Blount JD, Forbes S (2011) Patterns of egg yolk antioxidant co-variation in an avian brood parasite-host system. Behav Ecol Sociobiol 65:313–323. doi:10.1007/s00265-010-1048-3
Rubolini D, Romano M, Navara KJ et al (2011) Maternal effects mediated by egg quality in the Yellow-legged Gull Larus michahellis in relation to laying order and embryo sex. Frontiers Zool 8:24. doi:10.1186/1742-9994-8-24
Russell AF, Langmore NE, Cockburn A et al (2007) Reduced egg investment can conceal helper effects in cooperatively breeding birds. Science 317:941–944. doi:10.1126/science.1146037
Saether BE (1990) Age-specific variation in reproductive performance of birds. Curr Ornithol 7:251–283
Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci U S A 90:11446–11450. doi:10.1073/pnas.90.24.11446
Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A Physiol 114:271–276. doi:10.1016/0300-9629(96)00009-6
Scott DM, Ankney CD (1980) Fecundity of the brown-headed cowbird in southern Ontario. Auk 97:677–683
Scott DM, Ankney CD (1983) The laying cycle of brown-headed cowbirds: passerine chickens? Auk 100:583–592
Sealy S, Bazin R (1995) Low-frequency of observed cowbird parasitism on eastern kingbirds—host rejection, effective nest defense, or parasite avoidance. Behav Ecol 6:140–145. doi:10.1093/beheco/6.2.140
Strausberger BM (1998) Temporal patterns of host availability, brown-headed cowbird brood parasitism, and parasite egg mass. Oecologia 116:267–274. doi:10.1007/s004420050588
Strausberger BM (2001) The relationship of habitat and spatial distribution of nests with brown-headed cowbird parasitism of red-winged blackbirds. Wilson Bull 113:129–133. doi:10.1676/0043-5643(2001)113[0129:TROHAS]2.0.CO;2
Strausberger BM, Ashley MV (1997) Community-wide patterns of parasitism of a host generalist brood-parasitic cowbird. Oecologia 112:254–262. doi:10.1007/s004420050308
Strausberger BM, Ashley MV (2005) Host use strategies of individual female Brown-headed Cowbirds Molothrus ater in a diverse avian community. J Avian Biol 36:313–321. doi:10.1111/j.0908-8857.2005.03323.x
Strausberger BM, Rothstein SI (2009) Parasitic cowbirds may defeat host defense by causing rejecters to misimprint on cowbird eggs. Behav Ecol 20:691–699. doi:10.1093/beheco/arp042
Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264
Tuero DT, Fiorini VD, Mahler B, Reboreda JC (2012) Shiny cowbird Molothrus bonariensis egg size and chick growth vary between two hosts that differ markedly in body size. J Avian Biol 43:227–233. doi:10.1111/j.1600-048X.2012.05596.x
Williams T (1994) Intraspecific variation in egg size and egg composition in birds—effects on offspring fitness. Biol Rev Cambridge Philosophic Soc 69:35–59. doi:10.1111/j.1469-185X.1994.tb01485.x
Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Philosophical Trans R Soc B: Biol Sci 364:1107–1115. doi:10.1098/rstb.2008.0238
Woolfenden BE, Gibbs HL, Sealy SG (2001) Demography of brown-headed cowbirds at Delta Marsh, Manitoba. Auk 118:156–166. doi:10.1642/0004-8038(2001)118[0156:dobhca]2.0.co;2
Woolfenden BE, Gibbs HL, Sealy SG, McMaster DG (2003) Host use and fecundity of individual female brown-headed cowbirds. Anim Behav 66:95–106. doi:10.1006/anbe.2003.2181
Yasukawa K, Lindsey-Robbins J, Henger CS, Hauber ME (2016) Antiparasitic behaviors of Red-winged Blackbirds (Agelaius phoeniceus) in response to simulated Brown-headed Cowbirds (Molothrus ater): further tests of the frontloaded parasite-defense hypothesis. Wilson J Ornithol 128:475–486. doi:10.1676/1559-4491-128.3.475
Acknowledgements
We would like to thank field and lab technicians (Emilie Ospina, Michael Olsta, Jason Newton, Caitlin Elkins, Eric Peterson, Victoria Lima, Ohad Paris, Andy Ondrejecht, Lauren Novak, Price Dickson, Shannon Darcy, and Morgan Helfrich) for their assistance in nest searching and preparing eggs for hormone analyses. Thanks to Tara Stewart for help in the field and feedback on the manuscript. Thanks to Steve Buck for access to the University of Illinois’ Vermillion River Observatory, Champaign County Forest Preserve District, Urbana Parks District and Derek Liebert, Vermilion County Conservation District, Forest Preserve District of Kane County, Forest Preserve District of DuPage County, and Illinois Department of Natural Resources for use of their properties. Funding was provided by the USFWS and IDNR Federal Aid in Wildlife Restoration grant numbers W-161-R and W-181-R to TJB, the Forest Preserve District of Kane County, and the Illinois Natural History Survey as part of a postdoctoral fellowship to LM. Eggs were collected under USFWS permit# MB31458B-0 to TJB.
Author contribution statement
LM, SJC, and TJB conceived and designed the study. LM and SJC collected the data, RTP ran the hormone samples, and SJC and TJB performed the statistical analyses. LM, SJC, and TJB wrote the manuscript with editorial advice and feedback from RTP.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Christopher Whelan.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Merrill, L., Chiavacci, S.J., Paitz, R.T. et al. Rates of parasitism, but not allocation of egg resources, vary among and within hosts of a generalist avian brood parasite. Oecologia 184, 399–410 (2017). https://doi.org/10.1007/s00442-017-3870-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-017-3870-z