Journal of Zoology
Journal of Zoology. Print ISSN 0952-8369
THOMAS HENRY HUXLEY REVIEW 2011
Cuckoo adaptations: trickery and tuning
N.B. Davies
Department of Zoology, University of Cambridge, Cambridge, UK
Keywords
cuckoo; brood parasitism; co-evolution;
communication; deception.
Correspondence
Nicholas B. Davies, Department of Zoology,
University of Cambridge, Downing Street,
Cambridge CB2 3EJ, UK
Email: [email protected]
Editor: Steven Le Comber
Received 7 February 2011; revised 7 March
2011; accepted 8 March 2011
doi:10.1111/j.1469-7998.2011.00810.x
Abstract
I suggest that the cuckoo’s parasitic adaptations are of two kinds: ‘trickery’, which
is how adult cuckoos and cuckoo eggs and chicks evade host defences, and
involves adaptations that have co-evolved with host counter-adaptations, and
‘tuning’, which is how, once accepted, cuckoo egg and chick development are then
attuned to host incubation and provisioning strategies, and which might not
always provoke co-evolution. Cuckoo trickery involves adaptations to counter
successive lines of host defence and includes: tricks for gaining access to host nests,
egg trickery and chick trickery. In some cases, particular stages of host defences,
and hence their corresponding cuckoo tricks, are absent. I discuss three hypotheses
for this curious mixture of exquisite adaptation and apparent lack of adaptation:
different defences best for different hosts, strategy blocking and time for evolution
of defence portfolios. Cuckoo tuning includes adaptations involving: host choice
and monitoring of host nests, efficient incubation of the cuckoo egg, efficient
provisioning and protection of the cuckoo chick, and adaptations to avoid
misimprinting on the wrong species. The twin hurdles of effective trickery in the
face of evolving host defences and difficulties of tuning into another species’ life
history may together explain why obligate brood parasitism is relatively rare.
Introduction
The sight of a little warbler feeding a young cuckoo, 10 times
the warbler’s own body mass, has been a source of wonder
to human observers for thousands of years (Schulze-Hagen,
Stokke & Birkhead, 2009). Aristotle (384–322 BC), writing
some 2300 years ago, knew that the common cuckoo Cuculus canorus was a brood parasite: ‘it lays its eggs in the nest
of smaller birds’ (Peck, 1970). He also knew that the young
cuckoo ejected the host’s eggs and young from the nest:
‘when the young bird is born it casts out of the nest those
with whom it has so far lived’ (Hett, 1936). In his Natural
History of Selborne (1789), Gilbert White regarded cuckoos
as unnatural and ‘a monstrous outrage on maternal affection’. While Darwin (1859) was the first to explain how the
cuckoo’s parasitic behaviour could have evolved by natural
selection, even he referred to the young cuckoo’s ejection
instinct as ‘strange and odious’.
In this review, I suggest that the cuckoo’s parasitic
adaptations are of two kinds. The first, ‘trickery’, has been
well studied (Rothstein & Robinson, 1998; Davies, 2000;
Krüger, 2007; Kilner & Langmore, 2011). This involves the
various means, by which the cuckoo evades successive lines
of host defences in order to lay its eggs and to deceive the
hosts into treating the cuckoo egg and chick as one of their
own. These cuckoo tricks have co-evolved with host defences. However, success in trickery is only half the story.
Once the cuckoo egg and chick have been accepted, another
suite of adaptations is needed to ensure that their development is attuned to the host’s incubation and provisioning
strategies, which have evolved, of course, to optimize host
life histories. This second type of adaptation, ‘tuning’,
deserves more study.
I suggest that the twin hurdles, effective trickery in the
face of evolving host defences, and difficulties of tuning into
another species’ life history, may together help to explain
why obligate brood parasitism, though widespread across
the avian phylogeny, is a relatively rare strategy in birds,
occurring in just 1% of the c. 10 000 bird species worldwide.
These obligate parasities comprise: 57 species of cuckoos
(Cuculidae), five species of cowbirds (Icteridae), 17 species
of honeyguides (Indicatoridae), 20 species of African finches
(Viduidae) and one duck (Anatidae), the black headed duck
Heteronetta atricapilla from South America (Davies, 2000).
Here, I focus on the parasitic cuckoos to discuss parasite
adaptations in trickery and tuning.
The evolution of cuckoo parasitism
Currently, 141 species of cuckoos (Cuculidae) are recognized and the majority (60%) are parental species, which
build their own nests and raise their own young (Payne,
2005). A molecular phylogeny shows that obligate brood
c 2011 The Authors. Journal of Zoology c 2011 The Zoological Society of London
Journal of Zoology 284 (2011) 1–14 1
Huxley review 2011: Cuckoo adaptations: trickery and tuning
N.B. Davies
Figure 1 Mimetic, non-mimetic and cryptic
cuckoo eggs. (a) The host-race of the common
cuckoo Cuculus canorus specializing on reed
warblers Acrocephalus scirpaceus lays a mimetic egg (cuckoo egg on right, with three reed
warbler eggs), whereas (b) the host-race specializing on dunnocks Prunella modularis lays a
non-mimetic egg (cuckoo egg with four dunnock eggs). (c) Jacobin cuckoos Clamator jacobinus lay a non-mimetic white egg in the nest of
the cape bulbul Pycnonotus capensis. (d) The
shining bronze-cuckoo Chalcites lucidus plagosus lays a dark, cryptic egg in the dark, domed
nest of its host, the yellow-rumped thornbill
Acanthiza chrysorrhoa, which has pale eggs.
Photographs by: (a) Claire Spottiswoode, (b) W.
B. Carr, (c) Oliver Krüger, from Krüger (2011),
(d) Naomi Langmore.
parasitism has evolved independently three times within the
cuckoo family from parental ancestors (Sorenson & Payne,
2005). In most of the parasitic species, just like the common
cuckoo, the female lays one egg per host nest.
(i) New World cuckoos. The three species of parasitic
ground cuckoos from Central and South America parasitize
small passerine hosts with open or domed nests. The young
striped cuckoo Tapera naevia nestling has sharp bill hooks,
with which it slashes the host chicks to death (Morton &
Farabaugh, 1979). These are then removed by the host
parents, so the cuckoo chick is raised alone. The two
Dromococcyx species have not been well studied but there
are reports of host young disappearing soon after the
cuckoo chick hatches, so these nestling cuckoos may also
kill the host young (Payne, 2005).
(ii) Old World crested cuckoos. The four species of Clamator
cuckoos parasitize medium-sized to large passerines, including bulbuls, babblers, starlings, magpies and crows. The
cuckoo chick does not kill or eject the host eggs/young and
so it is often raised alongside host chicks (Payne, 2005).
Even so, the cuckoo often outcompetes the host young for
food, with the result that some are crushed or starve to death
(Redondo, 1993; Soler et al., 1995b). In these species, a
female cuckoo sometimes lays more than one egg (usually
just two) in the same host nest (Soler, 1990; Martinez et al.,
1998).
(iii) Old World cuckoos of the subfamily Cuculinae. This is
the largest group, comprising 50 species in eleven genera.
Most hosts are smaller than the cuckoo itself, usually
insectivorous species of moderate size (e.g. babblers and
shrikes) or of small size (e.g. warblers, chats, pipits, weavers,
sunbirds). In almost all of these cuckoos, the young cuckoo
ejects the host eggs or host young by balancing them on its
back, one by one, and heaving them out of the nest.
However, nestlings of the Asian koel Eudynamys scolopacea
do not eject, nor do those of the channel-billed cuckoo
Scythrops novaehollandiae (Payne, 2005). Both these cuckoos
2
parasitize hosts of a similar size to themselves (e.g. crows),
so ejection may either be too difficult, or the cuckoo may do
better if it is raised alongside some host young.
Trickery: successive stages
It is clearly costly for a host to raise a cuckoo chick because
the cuckoo either entirely destroys, or at least severely
reduces, the host’s own reproductive success. In theory,
therefore, hosts should evolve defences to thwart the cuckoo. These should select for cuckoo trickery, leading to
selection for improved host defences, further cuckoo trickery, and so on, a cycle of co-evolution where each party
evolves in response to selection pressure from the other
party (Dawkins & Krebs, 1979).
There are, indeed some remarkable examples of cuckoo
trickery, evolved to beat host defences, for example host-egg
mimicry (Fig. 1a), but equally there are surprising examples
where the hosts seem too easily fooled by cuckoo eggs and
chicks unlike their own (Fig. 1b,c). This curious mixture of
adaptation and lack of adaptation is an intriguing puzzle. I
first review the successive lines of host defences and cuckoo
trickery (Table 1), before considering why in some cases
particular host defences, and hence their corresponding
cuckoo tricks, are absent.
Cuckoo tricks for access to host nests
Female cuckoos invest a considerable time watching hosts
from concealed perches (Chance, 1940). Hosts may reduce
the chances that a cuckoo finds their nest by nesting further
from cuckoo vantage sites (Alvarez, 1993; Øien et al., 1996;
Moskát & Honza, 2000; Welbergen & Davies, 2009), by
concealing their nests (Moskát & Honza, 2000; Muňoz
et al., 2007), by secretive behaviour or unpredictable laying,
which would make it difficult for the cuckoo to time
parasitism effectively. Hosts may also reduce parasitism by
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Journal of Zoology 284 (2011) 1–14 N.B. Davies
Huxley review 2011: Cuckoo adaptations: trickery and tuning
Table 1 Cuckoo trickery in response to successive lines of host defence
Successive lines of
host defence
Host defences
Cuckoo trickery
Conceal nesting
attempt
Nest further from cuckoo vantage perches
Cryptic nests
Decoy nests
Unpredictable laying
Secretive behaviour
Monitor hosts to find nests and time parasitism
effectively
Nest defence
Increase surveillance and mob/attack female cuckoo to
prevent/dissuade nest inspection and laying
Secretive behaviour
Hawk mimicry
Nest closer to neighbours or in denser colonies
Polymorphism (reduces host recognition)
Male cuckoo lures hosts away to enable female to lay
Nest architecture to reduce parasitism (e.g. narrow
entrance tube)
Careful choice of nest.
Evolve smaller size.
Desert nest or increase egg rejection if cuckoo seen at
nest
Secretive and rapid laying
Reject foreign eggs
Host-egg mimicry.
Cryptic eggs
Supernormal eggs
Stronger egg shells
Destroy host clutch if reject cuckoo egg
Egg signatures
Mimic signatures
Reject foreign chicks
Host-chick mimicry
Chick signatures
Mimic signatures
Manipulative signals to exploit hosts
Vary defences in relation to parasitism risk
Rely on indirect as well as direct cues to parasitism
Secretive behaviour to minimize direct cues to hosts
Egg rejection
Chick rejection
All stages
their nest architecture, for example narrow entrance tubes to
their nests, which female cuckoos find difficult to enter
(Freeman, 1988; Davies, 2000).
Once a cuckoo approaches a host nest, the hosts may then
mob or attack it (Moksnes et al., 1991b; Røskaft et al.,
2002). In reed warblers, Acrocephalus scirpaceus, host pairs
that mobbed cuckoos strongly were less likely to be parasitized (Welbergen & Davies, 2009). Cuckoos may avoid
strong mobbers because of risks of injury (more likely with
larger hosts: Molnar, 1944). or because mobbing attracts
predators or other brood parasites (Smith, Arcese &
McLean, 1984; Krama & Krams, 2005) which increases the
chance that the cuckoo herself or her egg is depredated.
Mobbing also alerts neighbouring hosts (Welbergen &
Davies, 2008), who then may increase their mobbing of
cuckoos at their own nests (Davies & Welbergen, 2009).
Once hosts are alerted to the presence of cuckoos in their
neighbourhood, they increase nest attendance and egg rejection (Davies & Brooke, 1988; Moksnes et al., 2000; Bartol
et al., 2002; Davies et al., 2003). Nesting in a larger or denser
colony (Brown & Lawes, 2007) or closer to neighbours
(Welbergen & Davies, 2009) may reduce an individual host’s
parasitism risk through corporate vigilance or dilution.
Cuckoos counter these nest defences by secretive behaviour and rapid laying (Chance, 1940). They may also
benefit from hawk-like plumage, with cryptic upperparts
and barred underparts, which is more prevalent in parasitic
than in non-parasitic cuckoos (Payne, 1967; Krüger, Davies
& Sorenson, 2007), and which disuades close approach and
attack by hosts (Davies & Welbergen, 2008; Welbergen &
Davies, 2011). Some cuckoo species have polymorphic
female plumage, which may thwart enemy recognition by
hosts (Payne, 1967; Honza et al., 2006). In great spotted
cuckoos, Clamator glandarius, the male sometimes lures the
hosts away from the nest, which allows the female to avoid
host attacks while she lays (Davies, 2000). Co-operative
groups of carrion crows Corvus corone are less likely to be
parasitized by great spotted cuckoos, probably because the
presence of helpers allows the incubating female to spend
more time on the nest and so reduces the cuckoo’s free
access (Canestrari, Marcos & Baglione, 2009).
Cuckoo egg trickery
Evading host rejection
Early studies focussed on cuckoo–host interactions at the
egg stage, particularly egg mimicry by cuckoos (Baker, 1913;
Swynnerton, 1918). However, mimicry might be only one
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Huxley review 2011: Cuckoo adaptations: trickery and tuning
of three tricks that cuckoos employ to get hosts to accept
their eggs.
N.B. Davies
cuckoos are not selective when they remove an egg before
laying and simply pick an egg at random (Davies & Brooke,
1988; Langmore & Kilner, 2009).
Egg mimicry
The similarity between the eggs of the common cuckoo and
those of its hosts was first noted in the mid 18th century
(Jourdain, 1925; Schulze-Hagen et al., 2009). As has long
been suspected (Newton, 1893), the common cuckoo
species comprises several genetically different host-races
(Marchetti, Nakamura & Gibbs, 1998; Gibbs et al., 2000;
Fossøy et al., 2011). Each host-race tends to specialize on
one host species and lays a distinctive egg type that matches,
to varying degrees, the eggs of its particular host (Brooke &
Davies, 1988).
Recent studies reveal that host rejection and cuckoo egg
mimicry co-evolve. First, species of small birds with no
history of cuckoo parasitism (because of an unsuitable diet
or a nest inaccessible to female cuckoos) show little or no
rejection of foreign eggs, in contrast to cuckoo hosts which
often do reject eggs unlike their own (Davies & Brooke,
1989a,b; Moksnes, Røskaft & Braa, 1991a; Moksnes et al.,
1991b). Therefore, host egg rejection evolves in response to
cuckoo parasitism. Second, the perfection of matching of
cuckoo eggs to host eggs among the different races of the
common cuckoo is related to the strength of host rejection;
host species which show stronger discrimination against
eggs unlike their own are parasitized by cuckoo host-races
with better egg colour and pattern mimicry (Brooke &
Davies, 1988; Stoddard & Stevens, 2010, 2011). For example, reed warblers reject eggs unlike their own and their
cuckoo host-race has a mimetic egg (Fig. 1a), whereas
dunnocks do not reject odd eggs and their cuckoo host-race
lays a non-mimetic egg (Fig. 1b). Therefore cuckoo egg
mimicry evolves in response to host egg rejection.
A question still unresolved is whether differences in host
discrimination reflect equilibria, set by differences in the
costs and benefits of egg rejection to different host species,
or a continuing arms race, with younger hosts having poorer
rejection, and hence cuckoo host-races with poorer egg
mimicry (Stokke, Moksnes & Røskaft, 2005). Molecular
phylogenies to age the various cuckoo host-races might help
to answer this, but the picture is complicated because of
multiple origins of host-races and then imperfect host
fidelity (Marchetti et al., 1998; Gibbs et al., 2000; Fossøy
et al., 2011).
Egg crypsis
Other cuckoo species may counter host rejection not by egg
mimicry but by egg crypsis, laying dark eggs (Fig. 1d) which
hosts might find more difficult to detect, especially in darker,
domed nests (Brooker, Brooker & Brooker, 1990; Langmore
et al., 2009b). An alternative selection pressure for egg
crypsis is avoidance of detection by other female cuckoos,
who remove an egg before laying their own (Brooker et al.,
1990). Experiments are needed to test the importance of
these two selection pressures. Evidence to date suggests that
4
Supernormal eggs
In classic early ethological experiments, Baerends & Drent
(1982) made model eggs that herring gulls Larus argentatus
found even more attractive than their own eggs, because
they had certain ‘supernormal’ features, such as larger size
or finer speckling. It is possible that some cuckoos trick
hosts with supernormal eggs. For example, Alvarez (1999)
found that a host of the common cuckoo discriminated
against some non-mimetic eggs yet others that contrasted
markedly with their own were just as likely to be accepted as
highly mimetic eggs. Future work should test whether some
non-mimetic cuckoo eggs have features that hosts find
particularly attractive.
Egg signatures
Hosts not only evolve egg rejection as a defence, their egg
patterns evolve too, as distinctive ‘signatures’ to facilitate
the detection of parasite ‘forgeries’. Comparative evidence
supports this idea, which was first proposed by Swynnerton
(1918). Host species exploited by common cuckoos have less
variation in the appearance of eggs within a clutch, and
more variation between clutches of different females, than
do species with no history of cuckoo parasitism (Øien,
Moksnes & Røskaft, 1995; Soler & Møller, 1996; Stokke,
Moksnes & Røskaft, 2002). Both features make life more
difficult for cuckoos since it might be easier for hosts to
detect a foreign egg if all their own eggs look alike (Stokke
et al., 1999; Moskát et al., 2008; but for counter-examples,
see Kilner, 2006; Cherry, Bennett & Moskát, 2007) and
distinctive markings for individual host females makes it
harder for the cuckoo to evolve a convincing forgery for that
host species’ eggs (Takasu, 2003; Stokke et al., 2007).
A translocation by humans also shows that these two
features of host egg appearance evolve in response to
cuckoo parasitism. When African village weaverbirds Ploceus cucullatus were introduced onto two islands, where they
became isolated from their parasite, the diederik cuckoo
Chrysococcyx caprius, both within-clutch uniformity and
between-clutch variation declined over 60–100 generations,
and this compromised the weaverbirds’ ability to detect
foreign eggs (Lahti, 2005, 2006).
Host egg signatures are particularly spectacular in the
tawny-flanked prinia Prinia subflava, a common host of the
cuckoo finch Anomalospiza imberbis in sub-Saharan Africa
(Spottiswoode & Stevens, 2010). The prinia’s eggs vary in
four traits: colour (blue, white, red, olive), marking size,
variation in markings and marking dispersion. Experiments
involving placing foreign conspecific eggs into nests show
that the prinias are more likely to reject eggs unlike their
own and they pay attention to all four traits. Furthermore,
these four egg traits vary independently, which is exactly
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Journal of Zoology 284 (2011) 1–14 N.B. Davies
what would be expected if they had evolved to maximize the
distinctiveness of signatures.
The cuckoo finch has evolved similar variation in its eggs.
It would clearly pay individual female cuckoo finches to
target those prinia clutches for whom their egg would be a
good forgery. Perhaps this is simply not feasible because
cuckoo finches lay eggs at random and so suffer high
rejection rates as their egg is often a poor match (Spottiswoode & Stevens, 2010). This shows how effective host
signatures can be as a defence and raises the question of why
signatures are not similarly spectacular in all host species.
Perhaps other selection pressures, such as the advantage of
camouflage, constrain signature variation.
Egg shell strength
Some cuckoos and parasitic cowbirds have especially strong
shells (Spaw & Rohwer, 1987; Brooker & Brooker, 1991)
which are more difficult for hosts to puncture and reject
(Antonov et al., 2008). Hosts are then faced with the more
costly option of rejection by desertion. They may decide to
accept if cuckoo eggs are difficult to distinguish with
certainty (Antonov et al., 2009) or if acceptance is not too
costly, because the cuckoo egg is often laid too late, or some
host young can be raised alongside a cuckoo chick (Krüger,
2011). Host-races of the common cuckoo that encounter
stronger rejection from their host species have thicker
shelled eggs than those parasitizing less discriminating host
species, as expected if egg strengthening has evolved to
discourage host rejection (Spottiswoode, 2010).
Mafia enforcement
Finally, some brood parasites may disuade host rejection by
Mafia-like enforcement, punishing hosts who reject the cuckoo egg or chick (Zahavi, 1979). There is experimental evidence
for this in great spotted cuckoos (Soler et al., 1995c) and
brown-headed cowbirds Molothrus ater (Hoover & Robinson,
2007). In both cases, their hosts raise some of their own young
from parasitized nests so it might pay hosts to accept the cost
of raising a parasitic chick, to enjoy the benefit of some
personal reproductive success, rather than suffer the greater
net cost of clutch destruction. However, cuckoos which kill all
the host young are unlikely to be able to enforce acceptance as
these hosts gain nothing from a parasitized nest.
Cuckoo chick trickery
Early studies puzzled over why hosts of the common cuckoo
were so discriminating against eggs unlike their own, yet
readily accepted the cuckoo chick, which was larger and had
a different gape colour compared with their own chicks, two
cues (size and colour) readily used in egg discrimination
(Davies & Brooke, 1988).
One possible explanation is that chick discrimination is a
greater cognitive challenge. At the egg stage, hosts imprint
on their eggs the first time they breed and then reject eggs
that differ from this learnt set (Rothstein, 1975; Lotem,
Huxley review 2011: Cuckoo adaptations: trickery and tuning
Nakamura & Zahavi, 1995). If hosts are parasitized in their
first attempt, they will imprint on both their own and
parasite eggs, so there is a cost of misimprinting. Nevertheless, early learning brings a net benefit at the egg stage. In
an elegant model, Lotem (1993) showed that in theory such
a learning mechanism would not pay at the chick stage for
hosts of ejector cuckoos; if their first breeding attempt was
parasitized, they would imprint only on the cuckoo chick. In
subsequent, unparasitized attempts, therefore, they would
reject their own chicks. The greater cost of misimprinting at
the chick stage means that the rule ‘accept any chick’ would
do better than this imprinting rule. For hosts of non-evicting
parasites too, theory suggests that learned recognition of
brood parasite chicks is only likely to evolve under a
relatively rare combination of conditions, namely low host
chick survival in parasitized nests, high parasitism rates and
large clutch sizes (Lawes & Marthews, 2003). A second
challenge for chick discrimination is that, whereas eggs look
the same throughout incubation, chicks change dramatically
in appearance from day to day. With a brood hierarchy,
where chicks are at different stages of development, spotting
a stranger might be a difficult task (Davies & Brooke, 1988).
However, cognitive limitations cannot provide a universal constraint because recent studies reveal that hosts of
some Australian bronze-cuckoos (Chalcites spp.) do often
reject a cuckoo chick, either by abandoning it or by picking
it up and tossing it out of the nest (Langmore, Hunt &
Kilner, 2003; Sato et al., 2010; Tokue & Ueda, 2010). Single
host chicks tend to be accepted, so rejection of cuckoo
chicks is not simply a by-product of rejection of lone chicks.
Superb fairy-wrens Malurus cyaneus were more likely to
reject nestlings of an occasional parasitic cuckoo species,
which were less like their own young in appearance, than
nestlings of their regular parasite species, which tended to
resemble their own young. This suggests that visual cues
were involved in rejection. Furthermore, superb fairy-wrens
that accepted a cuckoo nestling did not then abandon a lone
fairy-wren nestling in later breeding attempts (Langmore
et al., 2003). Therefore hosts avoid the misimprinting
problem modelled by Lotem, perhaps by template-guided
learning to focus learning towards features of their own
young (Langmore et al., 2009a).
As predicted by co-evolutionary theory, in these cases
where hosts reject foreign young, the nestlings of their
respective cuckoo species have evolved visual mimicry of
the host nestlings in nestling down and colour of the skin
and gape flanges (Langmore et al., 2011).
Cuckoo nestlings sometimes also have begging calls
which are structurally similar to those of the host chicks
(McLean & Waas, 1987; Mundy, 1973; Payne & Payne,
1998; Langmore et al., 2008; Anderson et al., 2009b). Vocal
mimicry may also combat host rejection. However, experiments are needed to test this because begging calls like those
of host young may also be a case of ‘tuning’ to enhance host
provisioning (Kilner, Noble & Davies, 1999; Grim, 2005;
Madden & Davies, 2006). In non-ejector cuckoos, the nestling cuckoo has the opportunity to learn appropriate begging calls by listening to its host chick companions. Ejector
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cuckoos are not able to do this. Nevertheless, they may be
genetically predisposed to call like their host’s chicks (Langmore et al., 2008), and have the flexibility to modify their
calls through experience, homing in on those calls which
work best in stimulating host provisioning (Madden &
Davies, 2006; Langmore et al., 2008).
Minimizing parasitism cues
As cuckoos evolve improved trickery to combat these successive lines of host defence, this imposes increased costs on host
defences. For example, nest defence becomes more costly
when cuckoos mimic hawks, because the close inspection
necessary to recognize the enemy entails risks to adult host
survival. Likewise, when cuckoos evolve host-egg or hostchick mimicry, this introduces the costs of recognition errors
when hosts decide whether to accept or reject eggs or chicks
(Davies, Brooke & Kacelnik, 1996; Langmore et al., 2009a).
In response to these costs, hosts vary their defences in
relation to the local threat of parasitism, increasing nest
defence, egg rejection and chick rejection in places and at
times when parasitism is more likely (e.g. nest defence:
Lindholm & Thomas, 2000; Røskaft et al., 2002; Welbergen
& Davies, 2009; egg rejection: Brooke, Davies & Noble,
1998; Stokke et al., 2008; chick rejection: Langmore et al.,
2009a). This, in turn, selects for increased secrecy on the part
of the cuckoo, to minimize direct cues to parasitism.
Hosts may then respond to such increased cuckoo secrecy
in two ways. First, they may attend to their neighbours’
alarm responses, which increases the chance that they will be
alerted to cuckoo activity in their local area (neighbourhood
watch), and may also lead to improvements in their abilities
to discriminate cuckoos from other enemies through social
learning (Davies & Welbergen, 2009). Second, hosts may
rely more on indirect cues to parasitism, which are impossible for cuckoos to conceal (Holen & Johnstone, 2006), for
example distance to look-out perches, essential for cuckoos
when searching for host nests (see references above).
Trickery: adaptation and lack of
adaptation
The various cuckoo tricks described above make good sense
as responses to successive lines of host defence (Table 1). But
why are particular host defences, and hence their corresponding cuckoo tricks, sometimes absent? For example,
European hosts of the common cuckoo regularly reject
cuckoo eggs but usually accept cuckoo chicks (Davies &
Brooke, 1989b), whereas many Australian hosts do the
reverse, accepting cuckoo eggs yet rejecting cuckoo chicks
(Langmore & Kilner, 2010). I consider three hypotheses.
They may all apply together, in concert.
N.B. Davies
some of its clutch because the cuckoo usually removes one or
more host eggs before it lays (Davies & Brooke, 1988) or it
may puncture host eggs (Soler, Soler & Martinez, 1997; see
also Massoni & Reboreda, 1999; Spottiswoode & ColebrookRobjent, 2007). If the host delays further, until the chick stage,
it will have probably lost its entire clutch (ejector cuckoos) or
at least some of its clutch or brood (non-ejector cuckoos).
Even so, late rejection of single cuckoo chicks could still allow
a replacement clutch or save resources for the next season.
Costs and benefits of defence at different stages are likely
to vary between hosts. For example, nest defence will be
most effective for larger hosts (e.g. crows), which are better
able to drive a cuckoo away, or for hosts that can keep a
constant eye on their nest because they feed nearby. Many
hosts, however, will fail to detect the female cuckoo, so will
benefit from later defences. Hosts of ejector cuckoos will
benefit most from defences before the cuckoo chick hatches.
However, hosts with dark, domed nests may find it harder to
detect a cuckoo egg, so if the cuckoo wins at the egg stage,
there will be stronger selection for chick rejection (Langmore et al., 2003). The benefit of chick rejection, in turn, will
depend on future opportunities for breeding, and so on. A
comparative study of how host ecology and life histories
influence costs and benefits of successive lines of defence
would be illuminating.
Strategy blocking
In theory, success in one line of defence might reduce
selection for defences at another (earlier or later) stage, and
so block the evolution of another costly line, which would be
adaptive in its absence (Planqué et al., 2002; Britton,
Planqué, & Franks, 2007). A human analogy is effective
locks on the front door making investment in locks on the
bedroom door too an unnecessary luxury. This might help
to explain why we find egg rejection but not chick rejection
in European hosts and chick rejection but not egg rejection
in Australian hosts.
Likewise, strategy blocking might explain why some hosts
with effective mobbing responses to adult cuckoos then fail to
reject odd eggs from their nest and why, in turn, in these cases
there is no host-egg mimicry by the cuckoo (Fig. 1c). For
example, bulbul Pycnonotus capensis hosts of the Jacobin
cuckoo Clamator jacobinus have a strong first-line of defence,
in the form of mobbing, which not only makes it difficult for
the female cuckoo to gain access to the nest, but also makes it
difficult for her to monitor host behaviour, and so time her egg
laying correctly (Liversidge, 1970; Krüger, 2011). Thus many
cuckoo eggs are laid too late and fail to hatch. In this case egg
rejection is costly; the cuckoo egg is large, with a thick shell, so
the only option for the hosts is to reject by desertion. This may
not have evolved as a second line of host defence because of
the effectiveness of defence at an earlier stage (Krüger, 2011).
Different defences best for different hosts
In theory, early defences will bring greatest benefits. If a host
can prevent parasitism through nest defence, it saves its entire
clutch. If it delays defence until the egg stage, it will have lost
6
Time for evolution of defence portfolios
If some lines of host defence evolve first, and are then
effectively countered by the cuckoo, older cuckoo–host
c 2011 The Authors. Journal of Zoology c 2011 The Zoological Society of London
Journal of Zoology 284 (2011) 1–14 N.B. Davies
Huxley review 2011: Cuckoo adaptations: trickery and tuning
interactions will have had time for more sophisticated coevolved adaptations, perhaps with more lines, or later lines,
of defence and offence.
As an example of how ‘portfolios’ of defence (Britton
et al., 2007) might evolve, imagine a newly parasitized host
that attacks a cuckoo who approaches its nest, not as a
specific response to the threat of parasitism, but as part of its
general defence against intruders or predators. As a result of
the encounter, the host might have increased motivation to
inspect its nest and reject anything unusual. For example,
reed warblers increase their rejection of foreign eggs even
after the experience of a predatory jackdaw Corvus monedula at their nest . This rejection could then be refined as a
specific response to cuckoos, whose appearance would more
likely be followed by an odd egg in the nest. Thus, reed
warblers are more likely to reject an egg after they see a
cuckoo rather than a jackdaw at their nest (Davies &
Brooke, 1988).
This initial egg rejection could be adaptive even if the
hosts could not identify the cuckoo’s egg. Svennungsen &
Holen (2010) show that if the hosts are certain they have
been parasitized, then in theory it pays them simply to
reject an egg at random. This crude behaviour would then
expose the hosts to selection for egg discrimination and egg
signatures. The key point is that each change in host
behaviour creates a new arena of selection pressures, so
behavioural change drives the potential for genetic change
(Laland, Odling-Smee & Feldman, 1999). Thus defence
portfolios could evolve through ‘strategy facilitation’ (Kilner & Langmore, 2011), a counter-process to that of
‘strategy blocking’.
Tuning into host life histories
Once the cuckoo has by-passed host defences, it then has to
ensure that its egg and chick development are suited to the
host’s life history (Table 2).
Host choice
This first involves choosing hosts of a suitable size, diet and
nest type. Some hosts may have an unsuitable diet for
raising a cuckoo chick, or they may have nestlings that are
too large for non-ejector cuckoo chicks to compete with, or
nests that are too deep for ejector cuckoos to successfully
eject the host eggs (Grim et al., 2011). Then, there are suites
of adaptations to ensure that the cuckoo egg and cuckoo
chick are attuned to the host’s caring strategies.
Egg tuning
One suite of adaptations ensures that the cuckoo egg is
incubated efficiently and, ideally, hatches before the host’s
eggs. This makes life easier for ejector cuckoo chicks (host
eggs are probably easier to eject than host chicks) and also
gives non-ejector cuckoo chicks a head-start in development, so they are better able to outcompete the host chicks.
Time of laying is, to some extent, selected by host
defences and so is part of cuckoo trickery. Thus, cuckoo
eggs laid before the hosts have begun their clutch are more
likely to be rejected; very sensibly the hosts seem to follow
the rule ‘any eggs appearing before I begin to lay cannot be
mine!’ (Davies & Brooke, 1988; Langmore et al., 2003).
Nevertheless, timing is further refined by the need for
tuning. Eggs laid after the hosts have completed their clutch
are readily accepted but may not receive sufficient incubation. Various cuckoo adaptations ensure that the cuckoo
egg hatches in good time.
In common cuckoos, this suite of tuning adaptations
(Table 2) involves the female cuckoo timing her parasitism
to coincide with the host-laying period (Chance, 1940;
Davies & Brooke, 1988). She also depredates host clutches
too late to parasitize (where incubation has already begun),
which then makes the host’s replacement clutch available for
parasitism (Gärtner, 1981; Gehringer, 1979). It would be
interesting to know whether female cuckoos identify these
Table 2 Cuckoo tuning in relation to host life histories
Host characteristics
Cuckoo tuning
Size, diet and nest
Choose hosts of appropriate size, diet and nest for raising young cuckoo
Laying
Parasitize nest during host laying period
Depredate host clutches where incubation has begun to force hosts to lay replacement
clutch
Cognitive ability to remember the spatial and temporal availability of suitable host nests
Incubation
Match host incubation period by: small egg, internal incubation to give cuckoo chick a head
start, pecking host eggs to arrest their development
Host egg removal to ensure host incubation capacity is not exceeded
Chick provisioning
Either: (1) eject host eggs/chicks to claim all the food; (2) tolerate host chicks to increase
provisioning to the brood, with increased begging to claim unfair share
Begging display attuned to host provisioning strategies, or to exploit them
Alarm calls to warn nestlings of predators
Tune into host parent alarms
Imprint on host parents or brood mates to guide
species recognition or future mate choice
Avoid imprinting for species recognition (use innate password)
Imprint on hosts for future host choice
c 2011 The Authors. Journal of Zoology c 2011 The Zoological Society of London
Journal of Zoology 284 (2011) 1–14 7
Huxley review 2011: Cuckoo adaptations: trickery and tuning
advanced clutches by pecking eggs to test their stage of
development (as cowbirds do, Massoni & Reboreda, 1999),
or whether they use cues from host behaviour (e.g. incubation). Female great spotted cuckoos may peck host eggs to
arrest their development and ensure the cuckoo egg hatches
first (Soler et al., 1997). Greater honeyguides puncture host
eggs more when laying late relative to the host clutch, which
also increases the chance that the parasite chick hatches
(Spottiswoode & Colebrook-Robjent, 2007).
The small egg size of parasitic cuckoos, compared with
those of non-parasitic cuckoos, may also ensure the cuckoo
egg hatches in good time, as smaller eggs require less
incubation. Egg size, too, may partly be selected by host
defences, as hosts reject eggs that are much larger than their
own (Davies & Brooke, 1988; Langmore et al., 2003).
Nevertheless egg size may then be further refined to facilitate
tuning to host incubation or to produce a cuckoo chick with
the strength to eject host eggs (Krüger & Davies, 2004).
Some parasitic cuckoos lay at 48 h intervals. This may not
be a specific adaptation for brood parasitism, as nonparasitic cuckoos also lay at this interval. Nevertheless, this
gives the potential for the parasite egg to be incubated
internally inside the female’s oviduct for an additional 24 h
and so facilitates early hatching because the egg is laid with
embryo development already well underway. This ‘head
start’ in development has been shown for the common
cuckoo and the African cuckoo Cuculus gularis, and it also
occurs in greater honeyguides Indicator indicator, which also
lay at 48 h intervals (Birkhead et al., 2011).
A second problem concerning incubation tuning is that
the addition of a parasitic egg to the host clutch may exceed
the host’s incubation capacity. Female common cuckoos,
and other cuckoo species, usually remove one or two host
eggs before they lay. Egg removal does not increase host
acceptance of a parasitic egg (and is therefore not part of
trickery to deceive hosts) but is likely to improve its incubation efficiency (Davies & Brooke, 1988).
Finally, parasitic cuckoos are likely to need special
cognitive skills to enable them to remember the spatial and
temporal availability of suitable host nests (Clayton et al.,
2001). Female parasitic cowbirds (Molothrus spp.) have a
larger hippocampus than males, suggesting an adaptation to
enhance spatial memory (Sherry et al., 1993; Reboreda,
Clayton & Kacelnik, 1996). It is not known whether female
cuckoos have similar brain specializations, though on average brood parasitic cuckoos have smaller brains in relation
to their body mass compared with non-parasitic cuckoos
(Payne, 2005; Boerner & Krüger, 2008).
Chick tuning
A further suite of adaptations enhance the development of
the cuckoo chick (Table 2). In ejector species, the cuckoo is
raised alone and so it gains all the food the hosts bring to the
nest. Its problem is simply to ensure the hosts bring enough
food. Non-ejector cuckoos, on the other hand, have the
assistance of host chicks in soliciting food, but then have to
compete for the food once it is delivered. These alternative
8
N.B. Davies
strategies present different tuning problems and highlight
the two functions of begging signals, namely first to stimulate the delivery of food to the brood, and then to compete
for the food once it has arrived (Kilner et al., 1999).
Ejector cuckoos incur an energetic cost of ejection itself.
This includes the energy expended in evicting the host eggs
or young, and the time lost from soliciting food from the
host parents while evicting (Anderson et al., 2009a; Grim
et al., 2009). Once the cuckoo has eliminated competition
from the host young, it then has to work alone to stimulate
the host parents to bring it sufficient food. This involves
extravagant begging signals to increase host provisioning,
including rapid begging calls (Davies, Kilner & Noble, 1998;
Kilner et al., 1999), colourful gapes (Alvarez, 2004) or wing
patches to simulate extra gapes in the nest (Tanaka, Morimoto & Ueda, 2005; Tanaka & Ueda, 2005). Despite these
costs, ejector cuckoos grow better when they are raised
alone compared with when they are experimentally arranged
to share the nest with host young (Hauber & Moskát, 2008;
Grim et al., 2009).
Non-ejector cuckoos may tolerate host young either
because host egg ejection is too costly (large host eggs or
deep/large host nests makes ejection difficult: Grim et al.,
2009), or because the cuckoo gains a net benefit from the
presence of host young because their begging displays
stimulate increased provisioning by the host parents (Kilner,
Madden & Hauber, 2004). The cuckoo chick then takes an
unfair share of this extra food by stretching up higher,
begging first and by more elaborate begging, which manipulates the hosts into favouring it over their own young
(Redondo, 1993; Soler et al., 1995b). Experiments have
shown that brown-headed cowbirds (a non-ejector) increase
their growth rate by tolerating some host young when raised
by eastern phoebes (Kilner et al., 2004). Experiments are
needed to test whether non-ejector cuckoos likewise profit
by tolerating host young. Comparative studies would identify the host and parasite life-history variables that favour
ejection versus non-ejection by parasites.
In both ejector and non-ejector cuckoos, therefore, the
parasite chick usually begs more intensively than the host
chicks. It may be costly for the hosts to resist these super
stimuli because of the costs of ignoring signals from their
own young, which are likely to improve the host’s success in
unparasitized nests. For example, within their own broods,
the most intensive begging is likely to come from their most
needy chicks and their larger, fast-growing young are the
ones most likely to survive (Wright & Leonard, 2002). A
large, strongly begging parasite chick might therefore be
irresistable to the host parents.
Common cuckoos have a longer nestling period
(17–20 days) compared with the young of their host species
(11–14 days). In a population of reed warblers in the Czech
Republic, 16% of parasitized pairs deserted cuckoo nestlings when they were about 15 days of age (Grim, Kleven &
Mikulica, 2003). Reed warblers also deserted 22% of reed
warbler broods which were experimentally prolonged to
exceed their normal 11–12 day nestling period (by crossfostering younger chicks; Grim, 2007). This suggests that
c 2011 The Authors. Journal of Zoology c 2011 The Zoological Society of London
Journal of Zoology 284 (2011) 1–14 N.B. Davies
some host pairs reject common cuckoo nestlings not because
they recognize them as foreign, but because the cuckoo
demands more care than they expect to give to a normal
brood of their own (Grim et al., 2003). This would select for
limits to a cuckoo chick’s demands (better tuning to host
provisioning capacity), or manipulative begging to persuade
the hosts that extra investment was worthwhile (Redondo,
1993), or careful choice by the female cuckoo of high-quality
host pairs, who might be able to provide more care (Soler
et al., 1995a).
Finally, cuckoo nestlings may tune not only into host
provisioning strategies but also into the alarm calls that host
parents give to silence their own young when a predator
approaches their nest (Davies et al., 2006). Such alarmtuning may be particularly advantageous to cuckoos because their exuberant begging displays and prolonged nestling period are likely to increase their vulnerability to
predators.
Species recognition
We now come to a potential problem of ‘mis-tuning’. How
does a cuckoo know it is a cuckoo? Most species of birds do
not recognize conspecifics from birth but instead learn their
species characteristics during early association with their
parents and siblings. In theory, brood parasites could avoid
misimprinting by delayed social learning and the use of a
species-specific password-like cue to focus their learning on
conspecifics rather than their hosts. Such a password has
been discovered in brown-headed cowbirds, who use a
‘chatter’ call to associate with other cowbirds after fledging,
and then presumably learn more about their own species
(Hauber, Russo & Sherman, 2001). Brown-headed cowbirds
also use cues from their own plumage to form their recognition template for seeking out conspecifics (Hauber, Sherman
& Paprika, 2000). Experiments are needed to test whether
cuckoos, too, use passwords and self-referent phenotype
matching to avoid errors in species recognition.
Nevertheless, brood parasites do imprint on their hosts as
a guide to future host choice. This has been shown in the
parasitic Vidua finches of Africa (Payne et al., 2000) but it is
still unclear whether host choice by cuckoos develops
through imprinting on hosts or on their nest or habitat
characteristics (Teuschl, Taborsky & Taborsky, 1998). So
far, the difficulties of breeding cuckoos in captivity has
proved a barrier to experimental studies.
Trickery versus tuning
The distinction between trickery and tuning is often clear;
egg mimicry is trickery (non-mimetic eggs are rejected) while
internal incubation is tuning (it influences the time of
hatching, not acceptance). However, in other cases the
distinction is subtle. Hosts of bronze-cuckoos reject chicks
unlike their own, so mimicry of host young is trickery, which
enhances acceptance (Langmore et al., 2011). Hosts of
common cuckoos do not reject chicks unlike their own,
nevertheless a foreign chick may starve to death if its
Huxley review 2011: Cuckoo adaptations: trickery and tuning
begging calls are not attuned to the host’s provisioning
strategies (Kilner et al., 1999; Madden & Davies, 2006). In
the first case, non-mimetic chicks are abandoned or thrown
out of the nest. In the second case, mis-tuned chicks slowly
starve to death. In both cases the foreign chick dies, nevertheless the trickery tuning distinction focuses on the different mechanisms of host rejection. In the first case, a cuckoo
chick adaptation (mimicry) has co-evolved with host defences. In the second case, the cuckoo chick has evolved to
match the host’s provisioning rules, perhaps with no coevolved host response.
Trickery, therefore, clearly involves parasite adaptations
that have evolved to counter host defences, leading to coevolutionary changes in both hosts and cuckoos (Table 1).
Could parasite tuning also provoke co-evolution? In theory
hosts could escape parasitism by evolutionary changes in
many of the life-history features in Table 2, including: diet,
re-laying propensity, incubation, responses to egg removal
and provisioning strategies. Comparative studies would
reveal whether these potential changes have occurred (e.g.
Hauber, 2003). Fundamental changes in life history seem
less likely to evolve, or at least will take much longer, than
new behavioural defences. Nevertheless parasite tuning
could lead to evolutionary changes in hosts and hence
promote the evolution of further parasite adaptations. I
discuss two examples from other host–parasite interactions
to illustrate this.
Brood parasitic Vidua finch nestlings mimic the intricate
gape patterns of their host species’ young, with whom they
are raised. Classically, this is regarded as a case of parasite
mimicry evolved to avoid host rejection of foreign chicks,
with host nestlings evolving more distinctive signatures to
escape the parasite, and parasites evolving new forgeries.
However, there is little evidence that the estrildid hosts reject
chicks with mouth patterns unlike their own. An alternative
view is that the host nestlings’ elaborate mouth markings
have evolved through sibling rivalry to stimulate provisioning by their parents (Schuetz, 2005a,b). The Vidua parasite
nestling is then selected to tune into this communication
system, but with the twist that it will be selected to exaggerate the signals compared with the host young. This is
because the parasite’s demands will not be tempered by any
genetic stake in the other chicks in the nest, nor by the host
parents’ future reproduction. Once the parasite has exaggerated the signal, the host young will then be under selection to
increase their signalling in order to compete effectively for
care from their parents. This, in turn, will select for further
exaggeration by the parasite. So this might be a case where
the host chicks are evolving to match the parasite (Hauber &
Kilner, 2007). If so, this would be an example of parasite
tuning which has co-evolved with host responses.
A second example where parasite tuning might provoke
host counter-responses, and hence co-evolution, is the
puncturing of host eggs by the parasite. Female greater
honeyguides I. indicator usually puncture host eggs when
they parasitize a nest, which reduces the number of host
young that the honeyguide hatchling needs to kill (with bill
hooks) or outcompete. Spottiswoode & Colebrook-Robjent
c 2011 The Authors. Journal of Zoology c 2011 The Zoological Society of London
Journal of Zoology 284 (2011) 1–14 9
Huxley review 2011: Cuckoo adaptations: trickery and tuning
N.B. Davies
Table 3 Comparing cuckoo adaptations involving trickery versus tuning
Selection pressure
Function
Evolutionary process
Trickery
Tuning
Host defences
To avoid host discrimination (recognition and/or
rejection)
Co-evolutionary arms race involving host
defences and cuckoo trickery
Host life history
To increase host parental care
(2007) found that thicker and rounder host eggs were more
difficult for the female honeyguide to damage. Furthermore,
bee-eater Merops spp. and kingfisher Halcyon spp. hosts of
honeyguides have thicker egg shells than congeneric nonhost species, suggesting that host eggs have evolved stronger
defences in response to parasite puncturing. This would then
select for more efficient puncturing by the parasite.
In both cases, parasite tuning has provoked evolutionary
change in the host which, in turn, should select for changes
in parasite tuning. Therefore, the trickery-tuning distinction
becomes less clear when tuning provokes an evolved response in the hosts. If hosts, for example, evolve changes in
their parental strategies to avoid overexploitation by parasite chicks, then mis-tuning in the parasites might be the cue
that hosts use for discrimination. In this case, appropriate
tuning may be how the parasitic chick avoids detection and
so it becomes part of parasite trickery. Nevertheless, the
distinction is clear in terms of the different selection pressures and their functions in exploiting hosts (Table 3) and
may encourage more studies of the problems parasites still
face, once they have succeeded in tricking the hosts into
accepting the parasite’s eggs and chicks.
Acknowledgements
I thank Professor Nigel Bennett, Dr Steven Le Comber and
the Editorial Board of the Journal of Zoology for the honour
of writing this review. I thank Rebecca Kilner, Naomi
Langmore, Claire Spottiswoode, Martin Stevens, Cassie
Stoddard, Rose Thorogood and Justin Welbergen for comments and discussion, two anonymous referees for helpful
comments, and the Natural Environment Research Council
for funding our cuckoo research.
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