Common cuckoo offspring being fed by a reed

Common cuckoo offspring being fed by a reed warbler Brood Parasites Jody. Lee Estrada Duek, Ph. D With assistance from Dr. Gary Ritchison http: //people. eku. edu/ritchisong/matingsystems. html

Brood parasitism: Conspecific 1 • Intraspecific (or conspecific) brood parasitism – most prevalent among waterfowl but also reported in grebes, gulls, pigeons & doves, & songbirds (e. g. , Cliff Swallows, House Sparrows, & European Starlings) – increases when there is a shortage of nest sites & when population density is high – may reduce host fitness (if it responds by laying fewer eggs) – may be first step in evolution of obligatory brood parasitism [with occasional (or facultative) inter-specific brood parasitism the next step]

• Broods of mixed maternity, like this one, are common in Common Goldeneye and arise either through conspecific brood parasitism or amalgamation of broods after hatching. • The ducklings with different cheek colors were color marked at different nest boxes and thus originated from the nests of different females (photograph by B. Lyon; Lyon and Eadie 2000).

Family matters: Kin selection and conspecific brood parasitism • Conspecific brood parasitism is common in ducks; hosts often receive eggs laid by parasitic females of the same species • Andersson and Åhlund (2000) tested several aspects of a kin selection explanation for this phenomenon in Common Goldeneye (Bucephala clangula) – egg albumen sampling – statistical bandsharing analysis • They found that hosts and primary parasites were often related, with mean r = 0. 13, about as high as between first cousins. • Relatedness to the host was higher in nests where a parasite laid several eggs than in those where she laid only one. • Returning young females parasitized their birth nestmates (social mothers or sisters, which are usually also their genetic mothers and sisters) more often than expected by chance. • Such adult relatives were also observed together in the field more often than expected and for longer periods than other females. • Relatedness and kin discrimination - recognition of birth nestmates - play a role

Brood parasitism: Conspecific 2 • Andersson and Åhlund's (2000) findings contradict initial ideas. • conspecific brood parasitism has been viewed traditionally as an interaction that squarely pits the interests of the "parasite" against those of the host, leading perhaps to escalating coevolutionary arms races between them. • If, however, parasites and hosts are related, the argument reverses and what appeared to have been a parasitic exchange becomes, instead, a cooperative one not dissimilar from other well-known cooperative breeding systems (Lyon and Eadie 2000).

Obligate brood parasites 1 • always lay their eggs in nests of other birds • behavior has evolved independently at least 7 times • cowbirds (such as the Brown-headed Cowbird) & old world cuckoos are best known, but there are over 90 species of obligate brood parasites • Adaptations of brood parasites: – – – egg mimicry hard shelled eggs & destruction/removal of host eggs relatively small eggs relatively quick hatching baby brood parasites may dispose of competitor (e. g. , check this video)

Obligate brood parasites 2 table from Winfree 1999

Cuckoos and their hosts • The Old World family Cuculidae contains about 50 obligatory parasites, some of which are host generalists and some specialists. • The Common Cuckoo (Cuculus canorus) has an especially interesting pattern of host use: although it parasitizes over 100 species across its range, in any one locality only a few species are parasitized, and most individual female cuckoos use only one host species. • All the female cuckoos parasitizing one host species are referred to as a gens (plural, gentes). • Furthermore, some gentes lay eggs that mimic those of their host. Common Cuckoo (http: //www. nikon. co. jp) • A mechanism for the maintenance of this odd state of affairs was proposed a century ago: maternal inheritance of egg type combined with imprinting of the juvenile cuckoo on her host. • However, there is still no evidence to support this hypothesis (Winfree 1999).

A Chipping Sparrow (Spizella passerina, Order PASSERIFORMES - Family EMBERIZIDAE) shares it's nest with a huge Cowbird chick (Molothrus ater, Order PASSERIFORMES - Family ICTERIDAE). Photo: July 4, 2004. Miami http: //jrscience. wcp. muohio. edu/birds/ohio_birds/Cowbird_Nest_Parasitism. html Cowbird hosts and cowbirds • the cowbird is a generalist at the level of both the species and the individual. • Compared with the 50 species of parasitic cuckoos, there are only five species of parasitic cowbirds. • No evidence that cowbirds lays mimetic eggs • Many cowbird hosts accept these nonmimetic eggs. • Cuckoos have been brood parasites much longer (more than 60 million years) than cowbirds (2. 8– 3. 8 million years) (Winfree 1999).

Why do hosts tolerate parasitism? • On an evolutionary scale, if parasites benefit from brood parasitism and hosts are harmed by it, why do hosts tolerate parasitism? • Hosts can get rid of the parasitic egg in various ways, including ejecting the egg from the nest with their bill, building an additional layer of nest lining over the unwanted egg or abandoning the nest. • There are two primary hypotheses to explain why rejection is not universal among hosts of brood parasites

Hypotheses for Parasitism • According to the evolutionary lag hypothesis, hosts accept parasitic eggs because they have not yet evolved the ability to reject them. • Lag is an inherently unstable explanation: hosts would be better off rejecting, but at present they lack the necessary mutation, or selection has not had time to work on the genetic variation that exists. • According to the cost–benefit equilibrium hypothesis (also known as the cost– benefit balance or evolutionary equilibrium hypothesis), hosts accept parasitic eggs when the costs of rejection are greater than the benefits. • In its simplest form, cost–benefit equilibrium predicts a bimodal distribution of rejection frequencies; they should reject when benefits of rejection are greater than costs, and accept otherwise. • Clearly, there are benefits to rejecting a parasitic egg, but rejection can be costly: – First, the host might make a mistake and reject its own eggs (recognition error). – Second, could damage own eggs while removing the parasitic one (egg damage). – Third, the parasite could destroy nests from which the parasitic egg had been removed (the Mafia hypothesis). • Costs of the last two behaviors would increase with the frequency of parasitism, but the cost of the first might not (Winfree 1999).

Shining Bronze Cuckoo (Chrysococcyx lucidus) • • http: //people. eku. edu/ritchisong/matingsystems. html About 60% down the page – video of Shining Bronze Cuckoo eating

Yellow-billed cuckoo Cuckoo videos • Diederick’s cuckoo at Pete’s pond • • http: //www. youtube. com/watch? v=GXx 0 g 9 fo. LD 4 http: //www. youtube. com/watch? v=Nu. AD 5 z 5 Fz. E 4&feature=related • Finch feeding a cuckoo chick • http: //www. youtube. com/watch? v=IYLcfa 5 -PPI • Female cuckoo laying an egg, baby cuckoo • http: //www. youtube. com/watch? v=zc 75 ny. F 9 Tms

African village weaver birds A new study has demonstrated that African village weaver birds (Ploceus cucullatus) show less individuality in the appearance of their eggs when freed from the threat of raising the young of egg-mimicking diederik cuckoos (Chrsococcyx caprius). This suggests another clear example of natural selection driving evolutionary change in situ. African village weaver bird

Evolution of bird eggs in the absence of cuckoo parasitism 1 Diederik cuckoo • Historical introductions of species into new habitats create opportunities to test evolutionary hypotheses, such as the role of natural selection in maintaining traits. • Lahti (2005) examined two independent introductions of the African Village Weaverbird (Ploceus cucullatus) to islands where selection on egg appearance traits is expected to differ markedly from that of the source populations. • The color and spotting of village weaver eggs in Africa are highly consistent within clutches, but highly variable between individuals. • These features may be evolutionary response to brood parasitism.

Evolution of bird eggs in the absence of cuckoo parasitism 1 • In Africa, weavers are parasitized by each other and by the Diederik Cuckoo (Chrysococcyx caprius), an egg mimic. • African Village Weavers were introduced one century ago to Mauritius, and over two centuries ago to Hispaniola. • Both islands are devoid of egg-mimicking brood parasites. • In these two populations, between-individual variation and withinclutch consistency in appearance decreased, as has spotting • reductions more pronounced on Hispaniola: earlier introduction. • Such changes support the hypothesis that egg appearance is maintained by natural selection as a counteradaptation to parasitism. • These results illustrate that removal of an agent of selection can sometimes bring about rapid evolutionary consequences.

Village weaver eggs

Effect of brood parasites on their hosts • may greatly reduce reproductive success, particularly for relatively small hosts • large hosts (e. g. , Northern Cardinals) suffer some reduction in reproductive success (because female cowbirds may remove eggs) but are usually able to raise their remaining young to fledging

Cowbirds FEED ME! This Eastern phoebe nest has a parasitic intruder. The larger, redder gape belongs to the older parasitic brown-headed cowbird chick, while the smaller, paler gapes are the phoebe's own young. (Mark Hauber/UC Berkeley) • Young cowbirds join nestmates in making noise, then hog the food

Cowbird Nestlings • Young Brown-headed Cowbirds join nestmates in a begging chorus that brings in more food than one noisy cowbird chick could demand from its host parents • By eating more than their share, Kilner et al. (2004) found that cowbird chicks actually grow faster when sharing the nest and food with two host chicks than when alone in the nest • "The cowbird alone is incapable of bringing in enough parental resources - basically food - to be able to grow optimally, " said co-author Mark Hauber • "When it has nestmates, the whole nest brings in more parental care, because there is more begging altogether, and so the parents attend the nest more • But the cowbird monopolizes the feeding attempts by the parents • In our experiments, instead of getting 33% of the feedings (two host chicks and one cowbird chick) the cowbird got over 50% • the cowbird grew better with nestmates than when it was alone

Cowbird nestlings • Kilner et al (2004) switched eggs in Eastern Pheobe nests • They added a single cowbird egg to 20 nests, and after the chick hatched, they removed the host eggs from 10 • In the other 10 nests, after the cowbird hatched they placed two phoebe hatchlings of the same age or a day older • They then monitored the nests with video cameras to determine how often each chick ate, and daily for nine days weighed each chick • by day 8, cowbird chicks raised with two phoebe chicks were, on average, 14% heavier than cowbird chicks raised alone • brought food to nests with three hatchlings about four times each hour, versus 1. 5 times per hour for a lone cowbird chick • This strategy of sharing the nest to gain more resources appears to be successful generally among all the 100 or so species of birds parasitized by cowbirds

Why do hosts accept avian brood parasitism? 1 Prothonotary Warbler nest parasitized by a cowbird (Courtesy PNAS). Male Prothonotary Warbler (Protonotaria citrea) at a nest (Photo by Jeff Hoover). • Remember, the 3 theories regarding costs of rejection are: – First, the host might make a mistake and reject its own eggs (recognition error). – Second, could damage own eggs while removing parasitic one (egg damage). – Third, the parasite could destroy nests from which the parasitic egg had been removed (Mafia hypothesis).

Why do many hosts accept costly avian brood parasitism? 2 • parasitic eggs and nestlings often differ dramatically in appearance from the host • Scientists argue that evolutionary lag or equilibrium can explain this enigma • There is potential of parasitic birds to enforce acceptance by destroying eggs or nestlings of hosts that eject parasitic eggs • This retaliatory "mafia" behavior has been reported in one species of parasitic cuckoo but never in parasitic cowbirds • experimental evidence of mafia behavior in the brown-headed cowbird (Molothrus ater), a widely distributed North American brood parasite • manipulated ejection of cowbird eggs and cowbird access to predator-proof nests in a common host to test experimentally for mafia behavior • When cowbird access was allowed, 56% of "ejector" nests were depredated compared with only 6% of "accepter" nests • No nests were destroyed when cowbird access was always denied or when access was denied after we removed cowbird eggs, indicating cowbirds were responsible

Cowbird egg in a goldfinch nest Why do hosts accept costly avian brood parasitism? 3 • Nonparasitized nests were depredated at an intermediate rate (20%) when cowbirds were allowed access, suggesting that cowbirds may occasionally "farm" hosts to create opportunities for parasitism • Cowbirds parasitized most (85%) renests of depredated hosts • Ejector nests produced 60% fewer host offspring than accepter nests because of the predatory behavior attributed to cowbirds • Widespread predatory behaviors in cowbirds could slow the evolution of rejection behaviors and further threaten populations of some of the >100 species of regular cowbird hosts • Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs (Hoover & Robinson, 2007)

Click on the cowbird photo below to see a short video (wmv) of a female Brownheaded Cowbird removing eggs Female Brown-headed Cowbird removing an egg from a meadowlark nest

Host responses to brood parasites A Warbling Vireo removing the egg of a Brown-headed Cowbird from its nest (Underwood and Sealy 2006). • Most cowbird hosts accept parasitic egg with no defensive response • Some potential hosts actively defend nests against cowbirds (video), desert parasitized nests, bury cowbird eggs under a new nest floor, or eject cowbird eggs from parasitized nests • Much attention has recently focused on the effects of cowbird parasitism on neotropical migrants (paper)

Correlates of egg rejection in hosts of the Brown-headed Cowbird 1 • Peer and Sealy (2004) analyzed eight potential correlates of egg rejection in hosts of parasitic Brown-headed Cowbird (Molothrus ater) to test evolutionary equilibrium and evolutionary lag hypotheses as explanations for acceptance of cowbird parasitism. • Recall: – evolutionary lag hypothesis hosts accept because not yet evolved the ability to reject; lag is inherently unstable – cost–benefit equilibrium hypothesis (also known as the cost–benefit balance or evolutionary equilibrium hypothesis), hosts accept parasitic eggs when the costs of rejection greater than benefits • The analyses generally supported evolutionary lag.

Correlates of egg rejection in hosts of the Brown-headed Cowbird 2 • Historic contact with cowbirds may explain why hosts that have recently come into contact with cowbirds accept parasitism, but it does not account for acceptance by hosts with long histories of contact with cowbirds. • Egg predation by hosts, nest sanitation, population size, and egg appearance were not correlated with rejection. • Larger species that build larger nests were more likely to reject. • Large hosts may have been parasitized more frequently in the past, possibly due to their more easily found nests or superiority as hosts, and as a result, may have had more opportunity to evolve rejection.

Correlates of egg rejection in hosts of the Brown-headed Cowbird 3 • Rejection also correlated with taxonomic affiliation, suggesting once rejection evolves it is maintained; implies rejection is not costly and argues against evolutionary equilibrium. • Hosts with large bills more likely to reject. This may be a corollary of the tendency for large hosts, which tend to have larger bills, to reject. • An evolutionary equilibrium may exist for hosts with eggs that resemble cowbird eggs, depending on the costs to host reproductive success and likelihood of committing recognition errors. • Nevertheless, some hosts have been in contact with cowbirds for a long time, build large nests, have large bills, have a “favorable” phylogeny, and lay eggs that differ from cowbird eggs, yet accept cowbird parasitism. • Chance may play a role in the accumulation of the necessary recombinants and mutations necessary for the evolution of rejection.

A precocial nest parasite… how does that change things? • Attenborough cuckoo, cuckoo duck • http: //www. youtube. com/watch? v=4 Mb 0 GOITRUU&feature=related Brown headed gull