Brood Parasitism: An Alternative Life History

1. Brood Parasitism: An Alternative Life History N. B. Davies. 2000. Cuckoos, cowbirds and other cheats. Cambridge Univ. Press

2. Strong Parental Care: The Typical Avian Life History • Most birds live in pairs • Exhibit bi-parental care • Sex roles variable, but often near equal • Some species have uni-parental care • A few birds lack any “normal” parental care • Parental care can be stolen Dominion Power

3. Brood Parasitism The laying, or physical transport, of eggs of one species into the nest of a second species, where they receive parental care

4. Two Kinds of Avian Brood Parasites Facultative • “Lay” in own nest and nests of conspecifics • A common trait, especially in colonial and cavity-nesting species (E.g., starlings, snow geese, cliff swallows) Obligate • Lay only in nests of other species • 99 species in 5 families worldwide • 1% of all bird species

5. Obligate Avian Brood Parasites: 5 Taxa: 99 Species • Cuckoos - 57 of 130 Species • Probably evolved twice in the order • Honeyguides – all 17 species • Cowbirds – all 5 species • African parasitic finches – all 19 species • Black-necked Duck - 1 of 150 species

6. Cuckoos • Old and New World • Small hosts • Persistent, simple calls • Eat fruit and large hairy insects • In most species, cuckoo chick ejects host eggs/chicks • Often lay mimetic eggs

7. Honeyguides • Old World • Related to woodpeckers • Eat wax (bees nests) • Hatchlings kill host chicks with hooked beak • Guide honey badgers/people to bees Walter Weber Ian Jackson

8. African Parasitic Finches • Genus Vidua • Hosts in the related family Estrildidae • Specific host relations (mainly 1 host: 1 parasite) • Parasites reared with host chicks • Parasite chicks mimic host nestlings’ mouth markings, begging behaviour

9. Cowbirds • American blackbirds • Three North American Spp. • These 3 species are host generalists, prefer smaller hosts • Two specialize on other blackbirds • Parasites reared with host chicks

10. Black-headed Duck • Family Anatidae • Southern South America • Parasitizes other waterfowl, e.g. coots • Ducklings hatch before hosts • Independent at hatching • Ducklings need no parental care

11. Questions about the Brood Parasitic Life History • How did it evolve? • What trade-offs are involved? • What adaptations make brood parasites successful? • How can brood parasitism be countered by hosts?

12. How Did Obligate Parasitism Evolve? • From facultative brood parasitism? • Selection pressure created by time consuming feeding habits (like eating wax, hairy bugs) • In species that steal nests from other species? • E.g., Bay-winged “Cowbird” • Via communal nesting • E.g., Anis, Guira Cuckoos • During relaxed food limitation • Yellow-billed Cuckoos, periodical cicadas

13. Adaptations of Brood Parasites - 1 • Rapid laying (often when host absent) • Short incubation period • Brown-headed cowbird eggs hatch in 10-11 days vs. 12-14 d in hosts • Noisy begging behaviour • One cuckoo chick makes as much noise as a whole brood of reed warblers R. Kilner et al. Nature 397:667-672 (1999) • Predatory behaviours by • Adult great-spotted cuckoos, cowbirds http://biology.easternct.edu/People/elliott/htm • Nestling common cuckoos, honeyguides

14. Adaptations of Brood Parasites - 2 • Thick-shelled eggs • Resist puncture ejection • Egg mimicry • Foils rejecter hosts • Sharpens their egg discrimination • Removing eggs from host clutches while host is laying • May enhance parasite hatching success, especially in nests of large hosts • Superior spatial memory? (in females) D.F. Sherry et al. Proc. Nat. Acad, Sci. USA 90:7839-7843 (1993)

15. Defences by Hosts • Egg recognition and rejection • Inherited (American Robin) • Learned (Gray Catbird) • Costly – can reject own eggs • Desertion or burial of parasitized clutches • Yellow warblers build new nest cup • Aggression directed at parasite • Discrimination of foreign chicks • Little evidence of this except in estrildids

16. Why Prey on Host Nests? • The “Mafia” hypothesis Parasite “punishes” rejecting hosts: • Experimental evidence in magpies J. Soler et al. Evolution 49:770-775 (1995) • To synchronize host/parasite reproduction • Parasite benefits by “killing” unusable host clutches/broods • Host re-nests • Parasite then lays in new nesting attempt P. Arcese et al. Proc Nat. Acad. Sci. USA93:4608-4611 (1996)

17. Trade-offs? • Brood parasites: no control over kids’ fates • Eggs fail to hatch • Kids neglected by host parents • Maybe can lay more eggs? • Song Sparrow: 2.5 clutches /year averaging 3.5 eggs = 9 eggs/year • Brown-headed cowbird: an egg a day for 40-80 days = 60 eggs • Common cuckoo: 8 eggs • Yellow-billed cuckoo: 4-5 eggs • A two to six-fold fecundity advantage?

18. Tests of the Trade-off Hypothesis in Brown-headed Cowbirds • Find all host nests and count parasites/parasite eggs: to 17 eggs in 21d J. Smith & P. Arcese, Condor 96:916-934 (1994) • Study biology of reproduction • Counts of ovulated follicles in ovaries: 40-70 eggs D. Scott & C. Ankney, Auk 199:583-592 (1983) • Captive brown-headed cowbirds can lay 72 eggs • K. Holford & D. Roby, Condor 95:536-545 (1993) • Use genetic parentage analysis • Genotype female parents and all their offspring: 2.3 eggs/female B. Woolfenden et al., Animal Behaviour 66:95-106 (2003)

19. Status of Trade-off Hypothesis is Uncertain • According to the Woolfenden study, and a similar study by C. Hahn, brood parasites may lay fewer eggs than parental species • Biases in each type of study? • Need for further work

20. Our Local Parasite: the Brown-headed Cowbird

22. The Ultimate Host Generalist • 221 Host species overall • 170 Successful at raising cowbird • About 10% of hosts are rejecters • Many other host species desert • parasitized clutches • Seen as conservation villain • because of spectacular range • expansion since 1800

23. People’s Attitudes to Cowbirds • General public dislikes parasitic lifestyle • Birders dislike cowbirds, because • they see them as harming other birds • Biologists see the species • as a conservation villain • because of spectacular range • expansion since 1800 and • exposure to many new hosts

24. Cowbirds and Conservation • Range has doubled since 1750 • Prefers wooded habitats, avoids large forests • Can depress rare hosts, maintain numbers on common ones • Blamed for endangering four hosts • Kirtland’s Warbler • Black-capped and Least Bell’s Vireos • SW Willow Flycatcher • Suspected of negative effects on other hosts

25. Are Cowbirds Villains? • No hosts extirpated in range expansion • Most endangered hosts suffer from habitat loss/degradation • Long history of coexistence with many hosts HOWEVER, • Effect of cowbirds on host numbers are poorly known, with only one or two reliable estimates J. Smith et al. Ecology 83:3037-3047 (2002) • Managed more easily than other threats • Remain attractive “targets’ for managers

26. Unsolved Puzzles • How did obligate parasitism evolve? • Why are there so few obligate parasites? • 1% of birds • 2 % of ants • 1 Fish (Synodontis multipunctatus) High extinction rates in parasitic species? • Why is egg rejection so slow to evolve in cowbird hosts?

27. Summary • Obligately brood parasitic birds have a highly distinctive life history • Co-evolutionary “arms race” with hosts • Origin of obligate parasitism is uncertain • The local brood parasite, the Brown-headed cowbird, has a negative public profile with humans • Under some circumstances can be a severe conservation threat