Rutila, Jarkko
Brood parasitism in birds: coevolutionary adaptations in two cuckoo host systems. – University
of Joensuu, 2004, 88 pp.
University of Joensuu, PhD Dissertations in Biology, n:o 30. ISSN 1457-2486
Net version summary ISBN 952-458-554-7
Keywords: Brood parasitism, cuckoo, Cuculus canorus, redstart, Phoenicurus phoenicurus, brambling, Fringilla
montifringilla, coevolution, egg mimicry, rejection behaviour, interclutch variation, intraclutch variation.
Brood parasitism provides a good model system for studying coevolution. Cuckoo parasitism
causes great losses to host reproductive success as the newly hatched cuckoo chick evicts all of
its nest mates. Host adaptations against parasitism (rejection of non-mimetic eggs and
aggression towards the cuckoo) and the cuckoo’s counteradaptations (egg mimicry and cryptic
laying) are expected to be favoured by natural selection. The aim of this study was to explore
two different cuckoo-host systems and to explain how the different outcomes of a
coevolutionary arms race are shaped.
Both study species – the brambling, Fringilla montifringilla and the redstart, Phoenicurus
phoenicurus – are parasitised by the cuckoo, Cuculus canorus. In both systems hosts are
exploited by almost perfectly mimicking cuckoo eggs. Bramblings are good rejecters, also
ejecting conspecific eggs from their nests, while redstarts usually accept mimetic eggs and nonmimetic eggs are rejected at intermediate levels. Egg mimicry and rejection behaviour suggest
that there has been a long coevolutionary arms race between cuckoo and these two host species.
The results support the view that the host’s egg colour determines the differences in rejection
ability. The redstart’s eggs are an immaculate blue, and both intra- and interclutch variation in
egg appearance is low. This makes it easier for the cuckoo to develop perfect mimicry, which in
turn hinders the redstart’s ability to recognise and reject cuckoo eggs. Brambling’s eggs are
spotted and provide low intraclutch variation but high interclutch variation. Therefore the
cuckoo egg is not often a perfect match for host eggs, and it is easier for the brambling to detect
and remove the cuckoo egg from its nest.
The straightforward conclusion to be drawn from the above findings would be that the
brambling is a current winner in the cuckoo-host arms race, while the redstart is a loser.
However, peculiarities relating to the redstart-cuckoo system makes it more complicated. The
redstart is a cavity nester, which makes it harder for the cuckoo female to deposit her egg
properly in the host nest cup. In addition, the cuckoo chick fails to evict its nest mates in 50% of
cases. These phenomena reduce the cost of parasitism and make the acceptance of mimetic eggs
more favourable.
When the rejection behaviour of currently parasitised and unparasitised host populations
was compared, bramblings showed no interpopulation differences. The brambling results can be
explained by breeding nomadism and high gene flow between populations. However,
parasitised redstart populations ejected non-mimetic eggs by rejection (lower cost method),
while individuals in unparasitised populations ejected them by nest desertion (higher cost
method). The results from redstart populations indicate phenotypic plasticity or low gene flow
between populations. Different cuckoo-host systems may thus display different outcomes based
on several ecological factors.
Jarkko Rutila, Department of Biology, University of Joensuu, P.O. Box 111, FIN-80101
Joensuu, Finland
CONTENTS
1. INTRODUCTION
7
2. CUCKOO VERSUS HOST – THEORETICAL BACKGROUND
8
2.1. Cost for the host
8
2.2. Adaptations and counteradaptations in cuckoo-host systems 8
2.2.1. Evolutionary lag
9
2.2.2. Evolutionary equilibrium
10
2.2.3. The intermittent arms race hypothesis
11
2.2.4. The spatial habitat structure hypothesis
11
3. THIS STUDY
3.1. Aims of this study
4. MATERIALS AND METHODS
12
12
12
4.1. Study sites and study species
12
4.2. General methods
12
5. RESULTS AND DISCUSSION
13
5.1. Rejection rates in different host populations
13
5.2. Aggression towards the adult cuckoo
14
5.3. Peculiarities in the redstart-cuckoo system
15
5.4. The brambling-cuckoo system
17
6. CONCLUSIONS
19
Acknowledgement
20
References
21
List of original publications
This thesis is based on the following publications and some previously unpublished results.
The publications are referred to in the text by Roman numerals (I-V).
I
Rutila, J., Latja, R. and Koskela, K. 2002. The common cuckoo Cuculus canorus
and its cavity nesting host, the redstart Phoenicurus phoenicurus: a peculiar cuckoohost system? Journal of Avian Biology 33: 414-419.
II
Rutila, J., Jokimäki, J., Avilés, J.M. and Kaisanlahti-Jokimäki, M-L. Responses of
currently parasitized and unparasitized common redstart (Phoenicurus phoenicurus)
populations against artificial cuckoo parasitism. Manuscript submitted to Auk.
III
Rutila, J., Avilés, J. M. and Leech, D. Does the redstart Phoenicurus phoenicurus
escape cuckoo Cuculus canorus parasitism by selecting hole nests? Manuscript.
IV
Avilés, J. M., Rutila, J. and Møller A. P. Should the redstart Phoenicurus
phoenicurus accept or reject cuckoo Cuculus canorus eggs? Manuscript submitted to
Behavioural Ecology and Sociobiology.
V
Rutila, J., Vikan, J., Moksnes, A. and Røskaft E. Factors affecting brambling
Fringilla montifringilla rejection behaviour of parasitic eggs. Manuscript.
The publication is reprinted with permission from the publisher. Copyrights for publication I by
the Blackwell Publishing.
7
1. INTRODUCTION
“Wonderful and admirable as most
instincts are, yet they cannot be considered
as absolutely perfect: there is a constant
struggle going on throughout nature
between the instinct of the one to escape its
enemy and of the other to secure its prey.”
(Charles Darwin, in Romanes 1883).
Coevolutionary
adaptations
and
counteradaptations
have
interested
scientists since Darwin’s time. Our
knowledge of many fundamental biological
features can be improved by studying
coevolutionary processes. Coevolution can
be defined as specialised relationships
leading to reciprocal evolutionary changes
between interacting species (Thompson
1994). These interactions have a strong
influence on the population structure and
evolution of its members (Thompson
1994). Coevolution on a microevolutionary
time scale can be described as changes in
gene frequencies within populations. This
can be seen in the macroevolutionary
processes as a tandem co-speciation across
species (i.e. parallel cladogenesis), but it is
not a necessary outcome of coevolution
(Clayton & Moore 1997). Co-speciation is
sometimes even excluded from the
definition of coevolution.
Brood parasitism is an unusual
reproductive
strategy,
where
one
individual, the parasite, exploits the
parental care of another individual, the host
(Krebs & Davies 1993). Interactions
between parasite and host species take
place only over a short period of time (the
host’s breeding season), yet they have
strong
coevolutionary
responses
(Thompson 1994). One of the clearest
examples of microevolutionary changes
among vertebrates is to be seen in avian
brood parasitism (Lotem & Rothstein
1995). Under these circumstances it is
evident that co-adaptations between
parasitic birds and their hosts are a focus of
interest for many scientists. Avian brood
parasitism provides one of the best model
systems for studying coevolution among
vertebrates, because the costs of parasitism
impacts costs on host fitness and all the
critical interactions take place in the host
nest (Rothstein 1990).
Avian brood parasites can take advantage
of conspecific hosts (conspecific brood
parasitism, CBP) or individuals of different
species (interspecific brood parasitism).
CBP is commonly found among precocial
birds, especially in waterfowl, but also
many colony-nesting altricial species are
conspecific brood parasites (Yom-Tov
2001). Recent studies of CBP have focused
on the adaptive basis of this behaviour. It is
claimed that CBP can be a fitnessenhancing alternative reproductive tactic
(reviewed by Petrie & Møller 1991).
Another view is that individuals practising
CBP are making the best of a bad job
(Yom-Tov 1980). It has been suggested
that CBP is a precursor for obligatory
interspecific brood parasitism (Hamilton &
Orians 1965). CBP may also display a
range of variations. Sorenson (1998) has
documented
conditional
CBP
and
interspecific parasitism in two duck species
depending on environmental conditions.
On the other hand, interspecific brood
parasitism might evolve directly from a
nesting ancestor exploiting smaller host
species (Slagsvold 1998).
There are 90-95 bird species – from
seven unrelated taxa – that lay their eggs in
the nest of another species (Johnsgard
1997). This suggests that obligate
interspecific brood parasitism has evolved
independently at least five to seven times
during evolutionary history (Johnsgard
1997). Obligate interspecific brood
parasitism appears almost exclusively in
species with altricial offspring (the only
exception is the black-headed duck,
Heteronetta atricapilla, Payne 1977). One
possible reason for this is that birds with
altricial young benefit more than precocial
species from being obligate brood
parasites, due to a reduction in the high
8
costs of feeding nestlings (Lyon & Eadie
1991). The best-documented interspecific
brood parasitic systems are those of the
common cuckoo (Cuculus canorus) and its
hosts in Europe and Japan, the great
spotted cuckoo (Clamator glandarius) in
Europe and the brown-headed cowbird
(Molothrus ater) in North America.
2. CUCKOO VERSUS HOST
THEORETICAL BACKGROUND
–
2.1. Cost for the host
Inter – and intraspecific brood parasitism
has negative impacts on host fitness (Petrie
& Møller 1991). They both affect host
breeding success by reducing the host’s
hatching success, imposing egg and chick
loses and causing misdirected parental care
(e.g. Petrie & Møller 1991). These costs
are highly variable between species and are
dependent on the host-parasite system and
on the mode of development. Obligate
interspecific brood parasitism targeting
hosts with altricial young has a greater
negative impact on the host’s fitness than
does
conspecific
brood
parasitism
(Rothstein 1990, Davies 2000). This causes
rapid evolutionary responses from the host
and a corresponding retaliation by the
parasite (Rothstein 1975).
There are two distinct forms of
interspecific brood parasites with respect to
the cost they impose on the host: parasites
that remove host offspring and parasites
that are raised alongside host young. Brood
parasites that remove host young by
evicting or killing nest mates – like the
cuckoo – expose the host to extremely high
costs. Obviously, they prevent the host
from raising any offspring of their own
(e.g. Wyllie 1981). Even if the parasite is
identified and rejected, the parasitic female
will have removed one or two of the host’s
eggs at laying (Chance 1922, Wyllie 1981,
Brooker et al. 1990, Davies & Brooke
1998). However the most dramatic
reduction in host fitness occurs after
hatching, when the parasitic chick evicts
host eggs or small chicks from the nest
(Jenner 1788). These events usually reduce
the host’s breeding success to zero, leading
to rapid evolutionary cycles of adaptations
and counteradaptations between the
parasite and the host (Dawkins & Krebs
1979, Davies & Brooke 1988, Rothstein
1990).
Parasitic species that are raised alongside
the host offspring also have negative
effects on host fitness. The parasitic female
removes eggs from the host nest and
parasitic chicks may outcompete their nest
mates in the competition for resources
(Rothstein & Robinson 1998). The parasite
chick usually hatches first, develops
rapidly and has a size advantage, allowing
it to dominate parental care (Arias-deReyna 1998, Lichstenstein & Sealy 1998).
There is a new suggestion that parasites
enslave host young, using their begging
calls to persuade host parents to provide
increased provisioning, which the parasite
then monopolises (Kilner et al. 2004).
There is some controversial evidence that
chicks of giant cowbirds (Scaphydura
oryzivora) remove parasitic flies from the
host young and that the host receives actual
benefits from brood parasitism (Smith
1968). This is the only known example of
interspecific brood parasitism that has
some benefits for the host.
2.2. Adaptations and counteradaptations
in cuckoo-host system
Being subjected to such dramatic
reproductive costs, natural selection should
favour host defence against parasitism.
Rejection of parasitic eggs is the bestknown and a well documented form of host
anti-parasite behaviour (Rothstein 1990).
As
a
counteradaptation
to
host
discrimination of poorly matching eggs,
parasites have developed mimetic eggs
(Davies & Brooke 1988). The European
cuckoo (Cuculus canorus) has been the
subject of much study of rejection
9
behaviour. The acceptance of cuckoo eggs
is always maladaptive, given the species’
tendency to evict host offspring, and it is
striking that some host species do not show
any anti-parasite defences. One frequently
used cuckoo host in Britain, the dunnock
(Prunella modularis) does not reject any
parasitic eggs from its nest, no matter how
much they differ from its own (Davies &
Brooke 1989a). There are some host
species that are parasitised by cuckoo and
show high rejection rate of poorly
matching eggs (Davies & Brooke 1989a,
Moksnes et al. 1990). On the other hand,
most of the current cuckoo host
populations show an intermediate rejection
rate against non-mimetic eggs (Davies &
Brooke 1989a, Moksnes et al. 1990).
Many host species also behave very
aggressively towards adult cuckoos (e.g.
Moksnes et al. 1990). A host’s aggression
directed at the cuckoo differs from
aggression against a nest predator or hawk,
indicating that the host can recognise a
cuckoo as a special threat (Duckworth
1991). In addition, the rejection rates
correlate positively with aggression levels
across host species (Moksnes et al. 1990).
However, it remains unclear exactly what
the advantages of aggressive behaviour are,
since many small hosts are unable to drive
off the parasite (Wyllie 1981). Moreover,
brood parasites can use host aggression to
locate suitable nests for laying their eggs
(Seppä 1969). It has been suggested that
the host’s aggressive nest defence is
adaptive: seeing a cuckoo near the nest
increases rejection behaviour only in some
cuckoo hosts (Davies & Brooke 1988,
Moksnes et al. 1993), and this has led to
the cryptic laying behaviour of the cuckoo
(Davies & Brooke 1988).
These traits (rejection vs. mimicry,
aggression vs. cryptic laying) cause an
evolutionary arms race, in which the
parasites are constantly developing better
trickery strategies to exploit the hosts and
the hosts are constantly evolving better
defence mechanisms to avoid parasitism
(Dawkins & Krebs 1979). The cuckoo can
only reproduce by manipulating its host,
but the host has a good chance of future
reproduction, even if it sometimes fails to
escape cuckoo parasitism (Dawkins &
Krebs 1979). Since every cuckoo
encounters a host, but every host does not
encounter a cuckoo, the selection pressure
for cuckoo trickery is much stronger than
that for host defence (Dawkins & Krebs
1979). This explains why we can expect
the cuckoo always to be one step ahead in
the arms race (Dawkins & Krebs 1979).
Why certain host species, populations or
individuals exhibit acceptance or rejection
behaviour is a fundamental question in the
ongoing arms race between host and
parasite. Several hypotheses have been
proposed (reviewed by Stokke 2001).
2.2.1. Evolutionary lag
The evolutionary lag theory suggests that
every host species will eventually become
rejecters after sufficient time has elapsed
(Rothstein 1975, Brooke & Davies 1988).
Observed intermediate rejection rates are
the result of the slow spread of a rejecter
allele in the host population after low
parasitism pressure (Kelly 1987). There are
then three types of suitable cuckoo hosts
and they exhibit different rejection
behaviour towards parasitic eggs (Davies
& Brooke 1989a, b, Moksnes et al. 1990).
1. Suitable but rarely used hosts have high
rejection rate of foreign eggs (Davies &
Brooke 1989a, b, Moksnes et al. 1990).
They have been hosts in the past, but are
current winners in the coevolutionary arms
race and can no longer successfully be
parasitised by the cuckoo (Davies &
Brooke 1989 b). 2. Current hosts show
intermediate rejection rates and they are at
the stage where the rejection behaviour is
spreading to the whole population (Davies
& Brooke 1989b). The speed of this
process depends on the frequency of
parasitism (Kelly 1987). 3. Hosts that do
not reject non-mimetic eggs at all have
10
been hosts for a short period of time (Kelly
1987, Davies & Brooke 1989 b). Rejection
ability has not yet developed in these hosts
(Davies & Brooke 1989 b).
Some species are thought to be
unsuitable cuckoo hosts. These birds feed
their young by regurgitation or their diet is
unsuitable, they nest in places that are
inaccessible to cuckoo females or that
make the fledging of the cuckoo chick
impossible, or they have too large eggs or
too deep nests to allow the cuckoo chick to
evict its nest mates properly (Davies &
Brooke 1989a, b, Moksnes et al. 1990).
Unsuitable cuckoo hosts also show low
levels of rejection towards non-mimetic
eggs (Davies & Brooke 1989a, b, Moksnes
et al. 1990).
From the above information, Davies &
Brooke (1989b) have drawn the cycle of
cuckoo parasitism (Figure 1). In the first
step (stage 1) cuckoos start to exploit a new
host species by laying non-mimetic eggs in
their nests. At first the host has no rejection
ability. As the rate of cuckoo parasitism
increases, natural selection favours
individuals exhibiting rejection behaviour
(stage 2). As the rejection of non-mimetic
eggs spreads in the host population,
selection favours cuckoo individuals laying
mimetic eggs (stage 3). Alternatively, at
this stage the cuckoo can also move on to
an another naïve host that accepts its nonmimetic eggs. With mimetic eggs, the host
is faced with recognition problems: how to
separate the parasitic egg from its own
eggs? One solution involves the host
reducing intraclutch variation, making it
easier to spot the “odd one out” and
increasing interclutch variation in egg
appearance, thus preventing cuckoos from
developing perfect mimicry (Davies &
Brooke 1989b). Due to the costs of making
rejection errors, it may also pay the host to
accept a mimetic cuckoo egg (stage 4) if
the parasitism rates are not too high
(Takasu et al. 1993)
Figure 1. The coevolutionary sequence
between cuckoo and its hosts after Davies
(2000). The cuckoo-host arms race may
follow the suggested steps gradually, where
the cuckoo with no mimicry starts to
parasitise a naïve host (see text for details).
The study species of this thesis have been
included, showing their current status in
the cuckoo-host interactions.
2.2.2. Evolutionary equilibrium
The evolutionary equilibrium hypothesis
assumes that under some conditions
acceptance may be favoured over rejection
(i.e. the benefits of rejection are
outweighed by the costs, e.g. Takasu et al.
1993). There are three types of costs
relating to rejection behaviour that reduce
the benefits of rejection. Ejection costs
occurs when the host damages its own eggs
while rejecting the parasitic egg (Rothstein
1976, Davies & Brooke 1988, Moksnes et
al. 1991). This is most likely to happen
when a host with a small bill tries to eject a
parasitic egg by puncturing it (Davies &
Brooke 1988, 1989b, Rothstein 1976).
Rejection errors occur when a host ejects
its own egg instead of the parasitic egg
(Davies & Brooke 1988). Rejection errors
are expected to occur when the parasite
lays mimetic eggs (Davies & Brooke 1988,
Rothstein 1990). A recognition error means
that the host rejects its own egg or deserts
the nest when it has not been parasitised
11
(Rothstein 1982, Davies & Brooke 1988,
Marchetti 1992, Lotem et al. 1995). In the
cuckoo system it is only the recognition
errors that are important, because a
parasitised host will eventually lose all its
eggs anyway due to the cuckoo’s eviction
behaviour (Rothstein & Robinson 1998).
Hosts exhibiting intermediate rejection
rates may have the ability to adjust their
responses to the cuckoo egg in relation to
parasite density (Davies et al. 1996). The
prediction is that increased rejection
behaviour will be exhibited by individuals
who have seen a cuckoo near their nest. In
addition, hosts are more likely to make
recognition errors when they have seen a
cuckoo near the nest. However, a recent
study failed to find any evidence for
recognition errors in Acrocephalus
warblers (Røskaft et al. 2002a).
The host and parasite population may be
balanced so that cuckoos can successfully
exploit some individuals whereas other
individual hosts have strong defences
against parasitism. Such intrapopulation
variation may be age related. Experimental
evidence suggests that hosts learn to
recognise their own eggs by imprinting
(Lotem et al. 1995). Moreover, young birds
may accept any foreign egg in their first
breeding attempt because they have not yet
learned what their own eggs look like
(Davies & Brooke 1988, Lotem et al. 1992,
1995). This age related rejection ability
was demonstrated in one host species
(Lotem et al. 1992), but in two other
species, no such pattern of behaviour was
found (Stokke et al. 1999, Amundsen et al.
2002).
2.2.3. The
hypothesis
intermittent
arms
race
Differences in host rejection behaviour
following variation in parasitism pressure
between populations may cause cyclic
changes in parasitism, host abuse and
rejection rates (Soler et al. 1998). Parasites
may leave a host population with a high
rejection rate due to the low level of
benefits available (Soler et al. 1998). With
reduced parasitism pressure, rejection
behaviour will also decrease due to the
high costs to the host associated with such
behaviour (Davies & Brooke 1988, Rohwer
et al. 1989, Røskaft et al. 1990). The host
population becomes susceptible, and the
parasite can return. The parasites can then
re-colonise the formerly parasitised host
population after the rejection rate has
declined (Soler et al. 1998). Populations of
the great spotted cuckoo and its host, the
magpie (Pica pica), have demonstrated
local changes of this kind (Soler et al.
1998). However, some hosts of brood
parasites tend to retain a high level of
rejection even after parasitism has stopped
(Cruz et al. 1985, Post et al. 1990, Bolen et
al. 2000).
2.2.4. The
hypothesis
spatial
habitat
structure
Some host populations may be more prone
to higher levels of parasitism and suffer
increased costs to reproduction than other
populations (Lindholm 1999, Lindholm &
Thomas 2000). Cuckoos favour hosts
breeding in habitats that assist the cuckoo’s
ability to parasitise successfully (e.g. near
vantage points, Alvarez 1993, Øien et al.
1996). A highly parasitised population acts
as a sink, receiving new individuals from
unparasitised source populations (Røskaft
et al. 2002b). Arriving individuals do not
have rejection ability, and this slows down
the spread of the rejecter allele in the
parasitised population (Røskaft et al.
2002b). Species that utilise a range of
habitats for nesting across populations may
therefore exhibit intermediate rejection
behaviour (Røskaft et al. 2002b).
Species breeding in habitats that are
uniformly highly parasitised are typically
highly rejecting species (Røskaft et al.
2002b). However, differences in rejection
behaviour between host populations may
be due to phenotypic plasticity rather than
12
to genetically determinate factors (e.g.
Soler et al. 1994, Lindholm 2000). The
hosts may simply monitor cuckoo activity
in their local area and adjust their rejection
behaviour on the basis of this information
(Davies 2000).
3. THIS STUDY
3.1 Aims of the study
The aim of this study is to explore the
coevolutionary interactions between the
cuckoo and two of its hosts. In particular,
the aim is to study what factors affect the
rejection behaviour of these hosts. Both
cuckoo-host systems exhibit almost perfect
egg mimicry, yet their responses to cuckoo
parasitism are dramatically different.
The redstart (Phoenicurus phoenicurus)
and
the
brambling
(Fringilla
montifringilla) are two of the main cuckoo
hosts in Finland (Wasenius 1936, J. Rutila
unpubl.). Both species are parasitised by
means of mimetic eggs (Wasenius 1936),
and at least moderate rejection rates are
shown (e.g. von Haartman 1981, Järvinen
1984, Braa et al. 1992, I, II). These species
are dissimilar in many of their ecological
features (nest site selection, egg
characteristics),
thus
creating
an
opportunity to study the factors that cause
differences in responses to cuckoo
parasitism. I explore reasons why the
cuckoo seems to be the current winner in
one system and the loser in another.
4. MATERIALS AND METHODS
4.1. Study sites and study species
The redstarts were studied in North Carelia
in eastern Finland (62° 37' N, 29° 45' E) in
1984-2003. Two sites in stands of mature
Scotch pine forests were used. In 2003
additional data were collected from
northern Finland near the town of
Rovaniemi (66° 29' N, 25° 43' E). The
study sites were laid out in a similar
fashion.
The bramblings were studied in Tana in
northern Norway (70° 14' N, 28° 27' E) in
the breeding season of 2003. The study was
conducted in a mountain birch forest
during an autumnal moth outbreak,
providing an unusually high density of
bramblings.
Both study species are small migrant
passerine birds. The redstart is considered
the main host of the cuckoo in Finland,
whereas the current status of the brambling
as a cuckoo host is not well studied. The
nest record cards suggest that the
brambling is frequently parasitised in
northern Finland (J. Rutila unpubl.).
4.2. General methods
Data on parasitism rates were collected
from redstart populations over a period of
20 years (I). This long-term study enabled
assessment of the costs related to cuckoo
parasitism at population level. Moreover, it
revealed the variation in parasitism
pressure over the years.
Host
nests
were
experimentally
parasitised, and subsequent rejection
behaviour was observed. Redstarts were
parasitised during the laying stage by using
artificial cuckoo eggs made of plaster and
painted to resemble mimetic or nonmimetic eggs (I, II). It can be argued that
the artificially made mimetic blue eggs
have a different reflectance, especially in
the UV regions of the spectrum, compared
with genuine parasite eggs. However, when
measured with a spectroradiometer, the
mimetic artificial eggs had a fairly similar
reflectance compared to that of real cuckoo
eggs (J. Avilés unpubl.). Moreover, UV
reflectance did not seem to have any affect
on the redstarts’ rejection behaviour (J.
Avilés and J. Rutila unpubl.). However, the
colour of the mimetic artificial eggs
differed from real cuckoo eggs and redstart
eggs, and this could have caused higher
13
rejection rates of mimetic models than of
real cuckoo eggs.
Bramblings were parasitised with foreign
conspecific eggs after clutch completion
(V). Conspecific eggs were used to provide
more equal distribution between rejecters
and acceptors, because bramblings reject
mimetic models at very high rate (Braa et
al. 1992). The host reactions against
parasitic eggs were followed up to six days.
The host response was then categorised as
acceptance,
ejection
or
desertion.
Depredated nests were not included in any
of the analyses. The cuckoo dummy was
presented at hosts’ nests to explore their
reactions to an adult brood parasite.
Brambling clutches were photographed
by the standard method. Intraclutch
variation was assessed by six experienced
tests persons on the basis of these
photographs (from 1 to 5; 1 = no variation,
5 = all eggs look different). The contrast
between the parasitic egg and the host’s
own eggs was also evaluated by a similar
method (1 = no contrast, 2 = medium
contrast and 3 = maximum contrast).
5. RESULTS AND DISCUSSION
5.1. Rejection rates in different host
populations
The parasitism rate of the redstart
populations studied varied from 0 to 64%
(I). The average rate was around 20%,
which is still much higher than the overall
parasitism rate in the whole country
according to nest record cards (3.0%, n =
2157). This indicates that parasitism
pressure varies temporally and spatially in
different host populations. The differences
in the parasitism rate between populations
could cause dissimilarities in rejection
behaviour towards cuckoo eggs (Lindholm
1999, Lindholm & Thomas 2000).
The unparasitised redstart population in
Rovaniemi showed a rate of rejection
towards non-mimetic artificial cuckoo eggs
similar to that of the parasitised population
in Joensuu (II). However, in the Rovaniemi
population, redstarts rejected mimetic eggs
more frequently than in Joensuu (II). In the
Joensuu
population
rejection
was
accomplished by ejection, while in the
Rovaniemi population most rejecters
deserted their nests (II). Thus population
differences in host defence against
parasitism were masked by their method of
rejection. The difference in parasitism
pressure could explain these results, since
the unparasitised population showed the
more costly antiparasite behaviour. The
population that had been frequently
parasitised
responded
to
artificial
parasitism by a more sophisticated method.
It remains unexplained why the
unparasitised population still rejected
mimetic eggs more often than did the
parasitised population. This could be a
result of historic events connected with
mimetic cuckoo parasitism in the
Rovaniemi population or to the gene flow
between populations. The Rovaniemi
population may have been parasitised by
the cuckoo in the past. The cuckoo has
moved on to exploit other populations with
lower rejection ability, and rejection
behaviour has been retained in the
Rovaniemi population. Unfortunately no
data are available to explore these features.
The bramblings rejected conspecific eggs
at a similar rate in the currently parasitised
population in Tana (V) to those of an
unparasitised population in CentralNorway studied by Braa et al. (1992).
There was no difference in the method of
rejection either, both populations’ mainly
ejecting parasitic eggs (V). These
similarities can be explained by the
nomadic lifestyle of bramblings. Birds tend
to breed at high densities in areas with a
great abundance of prey items, for example
during
moth
outbreaks,
causing
populations to remain fluid in composition
(e.g. Silvola 1967, Linström 1987, Hogstad
2000). The gene flow between populations
under these circumstances should be high,
and rejection behaviour could be evenly
14
distributed across the whole range of the
species (Braa et al. 1992).
5.3. Peculiarities in the redstart-cuckoo
system
5.2. Aggression towards the adult cuckoo
The redstart is a cavity nesting species,
providing a unique cuckoo-host system to
study amongst the most common cuckoo
hosts. Cavity nesting hosts incur lower
costs from brood parasitism than open
nesting hosts (I, IV). Firstly, the redstart
cuckoo’s laying behaviour differs from
those gentes that target other host species.
Female cuckoos parasitising, for example,
meadow pipits (Anthus pratensis) or reed
warblers usually remove one or more host
eggs before laying its own egg (e.g.Chance
1940, Wyllie 1981, Moksnes et al. 2000).
In the redstart nests, host eggs are never
removed during cuckoo parasitism (I).
The redstarts showed low levels of
aggression towards cuckoo dummies at
their nest when compared with many other
frequently used cuckoo hosts (Figure 2). Of
the 26 experimental nests, only four
(15.4%) of the redstarts behaved
aggressively towards the dummy (J. Rutila
unpubl. results). When compared across
species, these values indicate that the
redstart has lower aggression levels in
relation to its rejection rate than any other
rejecting cuckoo host. If the redstart
aggression data from Moksnes at al. (1990)
is included (N = 6), the ratio is still the
second lowest after the reed warbler
(Acrocephalus scirpaceus).
However the aggression levels of
redstarts may be overestimated, because
redstarts behaved rather cryptically near
their nests during the egg laying stage. It
was impossible on many occasions to say
whether the host had seen the cuckoo
dummy in the vicinity of the nest. This
problem can be avoided by introducing
dummies after clutch completion, when
redstarts are always on their nests.
Bramblings behaved very aggressively
when they saw a cuckoo near the nest (V).
This is consistent with the high rejection
rate of the species. The adaptiviness of
aggression is questionable as it did not
decrease during the incubation period,
when cuckoo parasitism is no longer a
threat to the brambling; nevertheless,
cuckoos can also be seen as conventional
nest predators, affecting losses at any stage.
More surprisingly the adult bramblings
continued to attack cuckoo dummies when
they had chicks in the nest.
Figure 2. The relationship between the
rejection rate of non-mimetic artificial
cuckoo eggs and aggression towards a
cuckoo dummy at the nest of 19 suitable
cuckoo hosts. (Rejection data from: Davies
& Brooke 1989a, Moksnes et al. 1990,
Brown et al. 1990, Moskat & Fuis 1999,
Stokke et al. 1999, Moskat et al. 2003a.
Aggression data from Røskaft et al. 2002b
table 1.)
The cuckoo female lays it eggs directly in
the host nest whenever it is exploiting open
nesting hosts (Chance 1940, Wyllie 1981).
The data from redstart nest boxes suggest
15
that cuckoo females are probably not
laying directly into the nest. Many cuckoo
eggs are found outside the redstart nest cup
(I). Experiments with mimetic artificial
cuckoo eggs and real cuckoo eggs hardly
ever affect ejection by redstarts (I, II).
However, seeing a cuckoo dummy near the
nest could perhaps cause a higher ejection
rate of mimetic eggs (see Davies & Brooke
1988, Moksnes et al. 1993).
The lack of egg removal and imperfect
egg placement by female redstartparasitising cuckoos reduces the cost of
parasitism to the host and the real
parasitism rate experienced by the host
(IV). However, the host pays the greatest
cost after the parasite chick hatches. A
cuckoo chick evicts all the eggs or young
nestlings from the host nest within the first
few days (Jenner 1788). Failures in
eviction behaviour have hardly ever been
documented with open nesting host
species. However, in redstart nests almost
half of the cuckoo chicks were unable to
remove all their nest mates (I). Mixed
broods containing both redstart and cuckoo
nestlings were often fatal for the cuckoo
chicks (I). Whereas the redstart had some
fledgling success in every mixed brood of
this kind (I).
I suggest that the cavity nesting
behaviour of the redstart serves to reduce
the cost of parasitism. The apparently low
impact of cuckoo parasitism on the
redstart’s breeding success must have some
kind of implications for cuckoo-host
interactions. After collecting observational
and experimental data from the cuckooredstart system, I draw following
conclusions.
Firstly,
the
observed
parasitism rates calculated by counting
nests containing cuckoo eggs overestimate
the realised parasitism pressure: 50% of
cuckoo eggs are laid outside the redstart
nest cup and are therefore not a threat to
the host (I). Of those eggs that do reach the
nest cup, are incubated and develop, 46%
fail to evict the host young, ensuring at
least some reproductive success for the
host (I). Of course, 54% of cuckoos do
evict, kill or outcompete all the host young,
and in such cases the host’s reproductive
success is zero (I). Acceptance is further
favoured because the redstart is parasitised
by means of highly mimetic cuckoo eggs
(IV). Mimetic eggs are harder for the host
to separate from its own eggs and thus they
impose recognition costs. However
recognition costs are not found in the
preliminary experiments with the cuckooredstart system (J. Rutila unpubl.). Good
mimicry can also deter individuals from
rejecting by nest desertion, which is a more
costly mode of rejection. The model,
parameterised
with
these
values,
determined that acceptance should be
favoured over rejection when the
parasitism rate measured by egg laying is
under 20% (IV).
It has been claimed that the blue cuckoo
egg has developed as a result of the strong
rejection behaviour of redstarts (Moksnes
et al. 1995). However, the blue cuckoo egg
is actually a better mimic of whinchat
(Saxicola rubetra) eggs (Moksnes et al.
1995, J. Aviles unpubl. data). The whinchat
is also regularly parasitised in Finland (J.
Rutila unpubl.), and its nesting habits
suggest that it could be a more suitable
cuckoo host than the redstart (Moksnes et
al. 1995). The fact that the gens
parasitising redstarts lays highly mimetic
eggs, coupled with the rejection of nonmimetic eggs by redstarts, still suggests
that cuckoos and redstarts have a long
coevolutionary history. However the
cuckoo’s breeding success in redstart nests
seems to be at a much lower level than is
sufficient to support the breeding
population (I). Might the relationship have
been different in the past? Siivonen (1935)
suggested that redstarts were originally
ground nesters. Such ground nests, also
seen today, are cavities such as holes under
roots or rocks. These are, however, more
accessible to female cuckoos, allowing
them to lay and properly position their eggs
in the nest cup, and enabling the cuckoo
16
chick to evict host eggs or chicks more
efficiently than from tree holes.
Perhaps cuckoos started to exploit
ground-nesting redstarts with good success,
even using non-mimetic eggs. After a rapid
spread of cuckoo preference for the naïve
host, selection started to favour
discrimination and rejection by redstarts.
This led to the development of mimetic
cuckoo eggs as a counteradaptation. At this
point redstarts had limited alternative
strategies, due to their immaculate blue
eggs. Generally, birds laying immaculate
eggs also show lower rejection rates of
non-mimetic cuckoo eggs and lower levels
of aggression towards a cuckoo dummy
near the nest (Table 1). Selection against
parasites should favour reduced intraclutch
variation and increased interclutch
variation in egg appearance. Birds with
immaculate eggs have lower intraclutch
variation than species having eggs with
markings and patterns (Table 2). Therefore,
it should be easier for a host to spot an odd
egg in its clutch. However, immaculate
eggs also have low interclutch variation
(Table 2), and this has assisted the
evolution of high avidity cuckoo egg
mimicry, which can be disastrous for
redstarts. The results presented in Table 1
and 2 should be regarded with caution, as
the species are used as independent data
points (Harvey & Pagel 1991). The
phylogeny of the species should be taken
account (Harvey & Pagel 1991), but due to
small sample size in the immaculate egg
group, this was not possible.
Table 1. Intra- and interclutch variation in egg appearance in passerine birds having
immaculate or spotted eggs. (Data from Øien et al. 1995, table 2) Mann-Whitney U-test.
Interclutch
Intraclutch
Immaculate
N mean SD
Spotted
N mean SD
Z
11 1.66 0.41
11 1.27 0.16
60 3.08 0.54
60 2.03 0.42
-5.113
-5.040
p
***
***
17
Table 2. Aggression against a cuckoo dummy near the nest and the rejection rate of nonmimetic artificial cuckoo eggs in relation to the egg characteristic (spotted versus immaculate).
(Rejection data from: Davies & Brooke 1989a, Moksnes et al. 1990, Brow et al. 1990, Alvarez
1999, Moskat & Fuis 1999, Stokke et al. 1999, Moskat et al. 2003a,b. Aggression data from
Røskaft et al. 2002b table 1.). Mann-Whitney U-test.
Aggression
Rejection
Immaculate
N mean SD
N
Spotted
mean SD
Z
4 10.25 11.92
5 14.56 16.96
25 51.15 32.41
30 48.31 36.35
-1.977
-1.657
Once a mimetic cuckoo egg has
developed, it provides a good match in
every redstart nest. Perhaps increased
interclutch variation takes too long to
develop in the case of immaculate eggs,
and instead, redstarts may have escaped
cuckoo parasitism by careful nest site
selection. Nesting holes and cavities in the
tree allow redstarts to avoid cuckoo
parasitism to a great extent and to reduce
the impact of successful parasitism. Indeed,
cuckoos prefer ground-nesting redstarts to
the tree cavity nesting redstarts (III). In
addition, the unparasitised redstart
population in Britain breeds more
frequently in ground cavities than the
Finnish parasitised redstart population (III).
However, this difference disappeared when
only natural nest sites were included (III).
Ground nesting may be common in Finland
due to the low availability of tree cavities
in many natural pine forests. Ground
nesting has thus opened a window for
successful cuckoo parasitism.
5.4. The brambling-cuckoo system
Unlike the redstart, the brambling has eggs
with markings and patterns. This provides
a system for studying experimentally how
intraclutch variation and contrast of the
parasitic egg relates to host rejection
behaviour. Analyses support the view that
p
0.048
0.098
the contrast of the parasitic egg with the
host clutch is the main factor driving
rejection behaviour by the host (V). This is
consistent with many previous studies that
have also shown that mimetic eggs are
more easily accepted than non-mimetic
ones (e.g. Davies & Brooke 1988, 1989a,
Moksnes et al. 1993). Thus, host rejection
behaviour has favoured cuckoo egg
mimicry (Kelly 1987, Takasu et al. 1993).
The level of intraclutch variation had
also some bearing on the rejection decision
of bramblings. Rejecting individuals had
lower variation in egg appearance within
the clutch than acceptors (V). Brambling
interclutch variation is high compared to
that of many other frequently used cuckoo
hosts (Øien et al. 1995). This prevents
cuckoo egg mimicry from being a good
match in every host’s nest. It has been
suggested that variations in egg
characteristics are developed, at least
partly, to avoid brood parasitism (Øien et
al. 1995, Soler & Møller 1996, Stokke et
al. 1999, Stokke et al. 2002).
Other variables, including time of the
breeding season and clutch size (indirect
criteria for age), had no affect on
brambling reactions to parasitic eggs (V). It
seems that host age is not important in the
rejection decision either. The introduction
of a cuckoo dummy near the nest had an
unexpectedly negative impact on the
rejection rate. Bramblings who had
18
experienced a cuckoo dummy near the nest
exhibited lower levels of subsequent egg
rejection (V). This result differs
substantially from those demonstrated by
Davies & Brooke (1988), Moksnes et al.
(1993) for other species and suggested by
Braa et al. (1992) for bramblings. Possible
explanations include an experimental bias
caused by using conspecific eggs or
recognition problems experienced by
bramblings in relation to stuffed cuckoos.
However, when similar experiments were
duplicated in the next breeding season the
dummy effect disappeared (J. Vikan
unpubl.)
Bramblings
rejected
introduced
conspecific eggs at a high rate (V). The
rejection of conspecific eggs is rarely
reported for any bird species (but see for
weaver birds (Ploceus); Victoria 1972,
Lahti & Lahti 2002; for bramblings and
chaffinch (Fringilla coelebs); Braa et al.
1992, Moksnes 1992, for the Australian
reed warbler (Acrocephalus australis);
Welbergen et al. 2003), and it could result
from a CBP rather than from cuckoo
parasitism. However, no evidence for CBP
in bramblings was found from this study or
in the literature. In such circumstances, it is
a mystery that cuckoos continue to exploit
a host with such rigorous rejection
behaviour. I suggest five explanations.
Firstly cuckoo eggs are perhaps attractive
to the host, because they are bigger and
more finely speckled (see Baerends &
Drent 1982, Alvarez 1999). However,
artificial cuckoo eggs, which are larger and
finely speckled, are rejected almost
unanimously by bramblings (Braa et al.
1992).
Another possibility is that acceptance is
favoured because of the high costs related
to rejection in some conditions (e.g. Takasu
et al. 1993). The cuckoo eggshell has a
higher density than the host egg (Brooker
& Brooker 1991), and this resilience could
increase rejection costs for the host
compared to the rejection of a conspecific
egg. Bramblings are puncture ejectors
(Moksnes 1992), and while pecking the
parasitic egg it could damage its own eggs.
If puncture attempts lead to damage of the
host’s own clutch, it would be preferable,
or at least beneficial, to desert the nest and
renest. However, renesting may be
restricted because of harsh climatic
conditions (e.g. Moksnes et al. 1993).
Therefore, the best option could be to
accept the cuckoo egg, because it is
possible that the cuckoo egg is infertile or
will not hatch for some other reason. The
explanation that the strength of the cuckoo
eggs prevents rejection is unlikely, because
bramblings are able to eject hard model
artificial eggs (Braa et al. 1992).
Host age and rejection ability may be a
balancing factor favouring acceptance in a
population (Lotem et al. 1992, 1995). The
brambling is a true selective ejector and it
‘knows’ what its eggs look like (Moksnes
1992). If this knowledge depends on
learning at the first breeding attempt,
young individuals will not know their own
egg appearance before laying the first
clutch. If the host is parasitised during this
first attempt, it would accept a parasitic
egg. However, no relationship between
host age and rejection behaviour in a
brambling population was found using
indirect ageing criteria (V).
One possibility is that the brambling
cuckoo lays more eggs than average
cuckoo gentes. By doing this it has the
opportunity to introduce at least some eggs
into the acceptors’ nests. This is more
likely if the cuckoo exploits bramblings in
areas of high host density with access to
many nests. It is also possible that a cuckoo
female can evaluate how well its eggs will
match the host eggs. The female then only
has to lay in the nests where its eggs have
good chances of being accepted.
6. CONCLUSIONS
The two host species studied have one
fundamental difference in their rejection
abilities: bramblings reject mimetic cuckoo
19
eggs while redstarts do not. Intuitively, this
suggests that the cuckoo is currently
winning in the redstart system, but losing
in the brambling system. However, the
cuckoo’s reduced breeding success in
redstart nest boxes suggests that such a
simple conclusion is not sustainable.
Cavity nesting has a negative effect on the
cuckoos’ laying and fledging success.
Furthermore, the redstarts’ own breeding
success is not so greatly reduced by
parasitism as in the case of other cuckoo
hosts. The importance of cuckoo parasitism
as a driving agent for redstart cavity
nesting is questionable.
The existence of brambling cuckoo is
unexpected, given the hosts’ extremely
high rejection rates. It is impossible to say
whether these remaining bramblingparasitising cuckoos are representatives of
the last generations or, merely locally
unlucky. More data are needed concerning
actual cuckoo parasitism rates and breeding
success from northern Finland or other
parts of the main brambling-cuckoo
distribution area, such as those provided by
Montell (1917), Wasenius (1936) and
Balatsky (1994).
Redstart acceptance and brambling
rejection of mimetic parasitic eggs could be
driven by their own egg characteristics.
Bramblings have low intraclutch variation
and high interclutch variation in egg
appearance, whilst redstart clutches have
low intra- and interclutch variation. The
main constraint on high interclutch
variation for the redstart seems to be the
immaculate egg. Some individuals do have
small brownish spots on their eggs (von
Haartman et al. 1963-72), but this is
unlikely to have widespread effects on the
host’s rejection behaviour. However, some
cuckoos parasitising redstarts also have
similar dots on their eggs (personal
observation). I suggest that variation in
host egg appearance is the major factor
affecting the cuckoo-host dynamics.
My conclusions can support either
evolutionary lag or equilibrium hypotheses.
Both study species may be subject to an
ongoing dynamic coevolutionary process
(the evolutionary lag), or they may be in a
balanced state (the equilibrium). The
spatial habitat structure hypothesis can also
explain the observed difference in rejection
behaviour between bramblings and
redstarts. Redstarts breed in cavities, which
are sometimes inaccessible for cuckoos,
whilst bramblings always breed in open
nests near trees, which are accessible to
cuckoos. The heterogeneity in breeding site
structure may affect the spreading speed of
rejecter alleles (Røskaft et al. 2002b).
The truth is that we can only see
snapshots of coevolution, and it is therefore
hard to test the dynamics of cuckoo-host
interactions. More studies in different host
populations under different parasitism
pressure are needed. Further data on the
rejection rates of a cuckoo host with
immaculate eggs (especially the whinchat)
would clarify the conclusions drawn here.
In
conclusion,
the
coevolutionary
interactions between cuckoos and their
hosts do not always follow the simple
model of Davies & Brooke (1989b).
Sometimes – driven by different ecological
features in a host breeding biology –
coevolution can take unexpected turns.
20
Acknowledgements
I wish to express my gratitude to my supervisors, professor Eivin Røskaft and Dr. Jorma
Sorjonen for the excellent guidance they gave me throughout this project. Jorma taught me
everything I know about behavioural ecology and birds. Eivin invited me to Trondheim and
gave me all the help that I needed to get things started. I am also most grateful to three other
Norwegian cuckoo experts: professor Arne Moksnes, Dr. Bård Stokke and especially Johan
Vikan, MSc. Johan worked with me in northern Norway, where we accomplished astonishing
results during just one month.
One of the most important persons affecting this thesis has been Jesús Avilés, who has done a
brilliant job by helping me with the field work, contributing new ideas and writing articles. I
would also like to thank other co-authors: Raimo Latja, Kimmo Koskela, Jukka Jokimäki,
Marja-Liisa Kaisanlahti-Jokimäki, Anders-Pape Møller and Dave Leech for their crucial help. I
would like to acknowledge Joah Madden for the critical comments he made on my thesis. Risto
A. Väisänen has been very helpful whenever I needed data from nest card records.
My sincere thanks go to the members of the Boy Biologists of Finland. Especially Jussi and
Mika are responsible for this thesis by introducing me to the cuckoo-redstart problems and
giving me fatherly advice during this project.
I would like to thank all the staff members of the Department of Biology: it has been a great
place to work. Harri Kirjavainen kindly manufactured artificial eggs and skilfully prepared
cuckoo dummies. Petri Koponen is thanked for solving the problems with computers. I am also
grateful to all my friends and colleagues, especially Kimmo, Mikko, Arto and Lasse, who made
sure my time at the department was enjoyable. Juha Haikola is thanked for the high quality
cover picture. Rosemary Mackenzie kindly checked my English.
I want to thank my mother, brothers, sister and other relatives for their sincere support to my
studies. I am especially grateful to my mother, who lent me her car so that I could investigate
cuckoos and their hosts properly. Finally I would like to thank Jaana and Touko for being there
when I most needed them. Jaana has showed an enormous amount of love, understanding and
patience, even when her husband was away for long periods studying cuckoos.
The Faculty of Science and the Department of Biology of the University of Joensuu
financially supported this study.
21
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