BIOL 427

Brood Parasitism: An Alternative Life History

N. B. Davies. 2000. Cuckoos, cowbirds and other cheats. Cambridge Univ. Press

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

Dominion Power

• A few birds lack any “normal” parental care

• Parental care can be stolen

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

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

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

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

Honeyguides • • • •

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

Ian Jackson

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

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

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

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?

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

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

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)

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

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)

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?

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)

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

Our Local Parasite: the Brownheaded Cowbird

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

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

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

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

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?

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