Transcript Brood Parasites

Common cuckoo
offspring being fed by a
reed warbler
Brood Parasites
JodyLee 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
Number
of
parasitic
genera
table from Winfree 1999
Number
of
parasitic
species
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=GXx0g9foLD4
http://www.youtube.com/watch?v=NuAD5z5FzE4&feature=related
• Finch feeding a cuckoo chick
•
http://www.youtube.com/watch?v=IYLcfa5-PPI
• Female cuckoo laying an egg, baby cuckoo
•
http://www.youtube.com/watch?v=zc75nyF9Tms
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! 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=4Mb0GOITRUU&feature=related
Brown headed gull