J. Avian Biol. 39: 663671, 2008
doi: 10.1111/j.1600-048X.2008.04359.x,
# 2008 The Authors. J. Compilation # 2008 J. Avian Biol.
Received 20 August 2007, accepted 13 March 2008
Common cuckoo Cuculus canorus parasitism, antiparasite defence
and gene flow in closely located populations of great reed warblers
Acrocephalus arundinaceus
Csaba Moskát, Bengt Hansson, Lilla Barabás, István Bártol and Zsolt Karcza
C. Moska´t (correspondence), Animal Ecology Research Group of the Hungarian Academy of Sciences, c/o Hungarian Natural History Museum,
Budapest, Ludovika te´r 2, H-1083, Hungary. E-mail: [email protected]. B. Hansson, Department of Animal Ecology, Ecology Building,
Lund University, S-223 62 Lund, Sweden. L. Baraba´s, Zoological Department, Hungarian Natural History Museum, H-1066, Budapest,
Baross u. 13, Hungary. Present address of LB: West Hungarian University, Faculty of Forestry, Wildlife Management Institute, Sopron, Ady E.
u. 5, H-9400, Hungary. I. Ba´rtol, Directorate of the Kiskunsa´g National Park, Kecskeme´t, Liszt F. u. 19, H-6000, Hungary. Z. Karcza,
Ringing Center of BirdLife Hungary, Budapest, Költö u. 21, H-1121, Hungary.
In Hungary an unusually high rate of parasitism on the great reed warbler Acrocephalus arundinaceus by the common
cuckoo Cuculus canorus has been maintained for at least the last one hundred years. We evaluated parasitism rate,
antiparasite defence and genetic differentiation among Hungarian great reed warblers at three sites located 40130 km
from each other, where hosts suffered from a high (4168%), moderate (11%), and almost no (B1%) parasitism. We
were especially interested in whether the level of antiparasite defence was related to the local parasitism rate, and, if not, to
understand why. There was no difference among the three sites in the responses to experimental parasitism by nonmimetic model cuckoo eggs (rejection rate 7182%), which can be explained by strong gene flow between populations:
there was low level of philopatry and no genetic differentiation in the region. Reproductive success of the host in the
heavily parasitised site was about 54% of that in the unparasitised site, indicating that long-term persistence of host
populations in highly exploited areas depends on continuous immigration.
Obligate brood parasites take no care of their own offspring,
and depend entirely on the host species to hatch and care
their young (Payne 1998). The common cuckoo (hereafter
‘‘cuckoo’’) Cuculus canorus is a widespread avian brood
parasite exploiting several passerine bird species in the
northern Palearctic (Wyllie 1981). A cuckoo chick normally
evicts the host’s eggs or nestlings from nest after hatching
(e.g. Wyllie 1981, Honza et al. 2007), reducing the
reproductive success of the host (e.g. Kleven et al. 2004).
For this reason cuckoo parasitism poses a severe cost for the
host (Davies and Brooke 1988, Øien et al. 1998), which in
turn selects for antiparasite defence, like egg rejection
behaviour (e.g. Davies and Brooke 1988, Moksnes et al.
1991). On the other hand, cuckoos adapt to the hosts, e.g.
by rapid egg-laying (Wyllie 1981) and refined egg-mimicry
(e.g. Davies and Brooke 1988, Moksnes and Røskaft 1995,
Honza et al. 2001, Moskát and Honza 2002, Avilés and
Møller 2004, Avilés et al. 2006, Cherry et al. 2007a,b). The
coevolutionary process between a host species and its brood
parasite is often regarded as a continuous arms race (e.g.
Dawkins and Krebs 1979, Davies and Brooke 1989,
Rothstein 1990, Moksnes et al. 1991, Davies 2000), which
is generally limited by the adaptability of the cuckoo
(Honza et al. 2004, Lovászi and Moskát 2004).
Cuckoo parasitism rate is generally low: often less than
10% (Brooke and Davies 1987, Moksnes and Røskaft
1987, Davies 2000), rarely between 2030% (Lotem et al.
1995, Rutila et al. 2002, Antonov et al. 2006a, 2007a), but
may occasionally go up to 50% (Schulze-Hagen 1992).
Such high levels can occur when parasitism has recently
started in a population, but often drop to low levels after a
period of a few years (Takasu et al. 1993, Nakamura et al.
1998, Takasu 1998). In very rare cases, high levels of
parasitism have been maintained for longer time periods, as
in some populations in Hungary (see below). The often
relatively low parasitism rate slows down the coevolutionary
process between the host and the brood parasite, as Røskaft
et al. (2002, 2006) suggested in the spatial habitat structure
hypothesis. Fluctuations in the level of parasitism in
spatially separated host populations could be expected on
the metapopulation level, where the host’s adaptations to
parasitism may also vary locally (Soler et al. 1998, Grim
2002, Røskaft et al. 2002, 2006). The coevolutionary
process can also be slowed down by high costs of defence
against parasitism relative to the benefits obtained (e.g.
Lotem et al. 1992, Lotem 1993, Davies et al. 1996).
Density of the host population proved to be a key factor in
comparison of parasitised and non-parasitised reed warbler
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Acrocephalus scirpaceus populations in a metapopulation
study in Europe (Stokke et al. 2007), and similarly, Alvarez
(2003) reported that parasitism rate of cuckoos in Spain
increased with higher density of rufous bush robins
Cercotrichas galactotes. Besides parasitism rate, antiparasite
defence of the host can also characterise a hostbrood
parasite relationship. Research in small isolated marsh
populations of reed warblers in Britain showed that the
antiparasite defence varied site-by-site (Lindholm and
Thomas 2000). In a large-scale comparison of magpie
Pica pica and its parasite the great spotted cuckoo Clamator
glandarius, a strong geographical component was found for
the spread of the rejecter gene (Soler et al. 1999, Martı́nGálvez et al. 2007).
Survival of host populations under heavy cuckoo
parasitism is problematic (Takasu et al. 1993, Barabás
et al. 2004). When frequency of brood parasitism is high,
reproductive success of the host may decline drastically, so
that the population turns into a sink population. This is
also the case in the brown-headed cowbird Molothrus ater
(Ward and Smith 2000), where the nestlings of the host
grow up together with the parasitic chick (e.g., Dearborn
and Lichtenstein 2002, Hauber and Dearborn 2003). The
cowbird chick often out-competes the host chicks (Kilner
et al. 2004), so the reproductive success might be lowered,
especially in small hosts (see also Lichtenstein and Sealy
1998). Similarly, there is a significant cost when cuckoo and
host nestlings grow up together, either naturally (Rutila
et al. 2002), or experimentally (Hauber and Moskát 2008;
but see Martı́n-Gálvez et al. 2005 for an alternative result).
Also feeding a single cuckoo chick is exhausting and costly
for the adult birds, and again especially for small hosts
(Butchart et al. 2003, Grim et al. 2003, Kleven et al. 1999).
Although antiparasite defence, e.g. egg rejection, lowers the
cost of cuckoo parasitism, counter adaptations of the
cuckoo reduce the efficiency of such antiparasite defence
mechanisms. However, the antiparasite defence also has
some cost since the host’s own eggs can mistakenly be
ejected or whole broods be abandoned (Davies and Brooke
1988, Lotem et al. 1995, Øien et al. 1999, Moskát and
Honza 2002, Stokke et al. 2002, 2005). Therefore the
survival of the host population is affected by both the
frequency of cuckoo parasitism and the levels of cuckoo and
host adaptations.
In the present study, we look for the solution to the
paradox of how host populations suffering from unusually
high cuckoo parasitism could survive for long periods of
time. In Hungary, there is an exceptionally high rate of
cuckoo parasitism on the great reed warbler Acrocephalus
arundinaceus; some populations seem to have had 50%
parasitism for at least one hundred years (Molnár 1944,
Moskát and Honza 2002). Results of computer simulations
suggest that the high levels of parasitism may be maintained
if the host has a metapopulation structure with both
parasitised and unparasitised populations. Then immigration from unparasitised host populations to highly parasitised populations could prevent the latter populations
from extinction, and create a relatively stable hostbrood
parasite relationship (Barabás et al. 2004). Here we evaluate
the validity of this model with real data from three
Hungarian great reed warbler populations located 40130
km from each other (Fig. 1). We compared the level of
664
antiparasite defense and degree of genetical similarity, and
evaluated the ability for self-reproduction of great reed
warbler populations in Hungary that suffered from different
degrees of parasitism (ranging from 1 to 50% parasitism).
When the density of the parasite is high, the main factor
affecting the rate of parasitism in great reed warblers is the
availability of trees close to host nests, providing vantage
points for the cuckoos (Moskát and Honza 2000; see also
Alvarez 1993, Øien et al. 1996, Antonov et al. 2006b,
2007b). Nest concealment might also serve as an important
mechanism to avoid brood parasitism (Schulze-Hagen et al.
1996, Moskát and Honza 2000, McLaren and Sealy 2003),
and nest predation (Ille et al. 1996, Schulze-Hagen et al.
1996, Batáry et al. 2004, Batáry and Báldi 2005).
We hypothesize: (1) that heavily parasitised great reed
warbler populations could persist for long periods of time if
immigration from unparasitised populations maintains
them. We predict that the reproductive success of great
reed warbler populations in treeless reed-beds, e.g. in inner
parts of lakes, should be much higher than in reed along
channels, which are bordered with treelines and thus suffer
from significant cuckoo parasitism. If reproduction rates in
unparasitised host populations are not significantly higher
than in the parasitised populations, the hypothesized
sourcesink dynamic system cannot easily explain the
survival of the parasitised host population (Barabás et al.
2004). (2) In the lack of large ecological barriers between
the study populations, gene flow is expected to be bidirectional, both from unparasitised to parasitised populations, and vice versa. In this way, rejecter genes may reach
unparasitised populations from parasitised populations. For
these reasons, we predict a high genetic resemblance and
similar rejection rates in parasitised and unparasitised host
populations, when tested with non-mimetic artificial
cuckoo eggs. If the second hypothesis is not true, i.e. if
the populations are genetically differentiated and adapted to
the local parasitism rate, we expect higher acceptance rates,
and consequently lower rejection rates in the unparasitised
populations, but lower acceptance and higher rejection rates
in the parasitised host populations.
Figure 1. A survey map of the three study sites in Hungary.
Material and methods
Study sites and field methods
The study was conducted in three study sites in Hungary
(Fig. 1): (1) Apaj Channels. This site was situated ca. 4060
km south of Budapest, in the surroundings of the villages
Bankháza and Apaj (478 7?N, 198 05?E), close to the town
Kiskunlacháza. The main channel, the ‘‘Dömsödi Árapasztó’’ flood-relief channel is connected to the Danube
River. Great reed warblers nested in the narrow, approx. 3
5 m wide strips of reed at both sides of channels. Lines of
trees at the banks offered high quality perching sites for
cuckoos at most parts of these channels. The parasitism rate
at this site was on average 56% over the study period
(19982003; range: 4168%). (2) Tisza River. Great reed
warblers were studied in channel-side reed-beds adjacent
with the Tisza River at the village Lakitelek (468 53?N, 208
00?E), close to the town Kecskemét, ca. 80 km south-east of
Budapest. At this site the parasitism rate was about 11%. (3)
Lake Velence. This site covered an extensive reed archipelago in a shallow lake (Báldi and Kisbenedek 2000) in the
surroundings of the summer resort Agárd (478 12?N, 188
32?E), close to the town Székesfehérvár, ca. 40 km southwest of Budapest. We observed no cuckoo parasitism in the
central parts of the lake, but we found one parasitised great
reed warbler nest at the shore, where there were trees serving
as vantage points for cuckoos. We estimate that the
parasitism rate on this great reed warbler population should
be lower than 1%. At this site great reed warblers cooccurred with reed warblers, but in Apaj Channels and
Tisza River other Acrocephalus warblers were almost absent
from channel-side reed-beds. The three study sites are
located 40130 km from each other (closest distances: Apaj
vs. Tisza: 80 km; Apaj vs. Velence: 40 km; Tisza vs.
Velence: 130 km; Fig. 1). The Apaj and Tisza sites are
situated in the Hungarian Great Plain, whereas the Lake
Velence site can be found in Trans-Danubia, a hilly area.
In Hungary, the great reed warbler seems to be a reed
edge species, preferring to occupy territories in the reed
water interface (Báldi and Kisbenedek 1999). The species
starts breeding in mid-May. The breeding season is
relatively long, with second or replacement clutches being
laid in early July. Most nests are however found in late May
and June. Our study was conducted between mid-May and
early July between 1998 and 2003 in Apaj Channels, in
2000 at Lake Velence, and in 2001 at Tisza River.
We used artificial cuckoo eggs to test egg discrimination
ability and acceptance/rejection rates of the populations,
following the protocol of Bártol et al. (2002) and Moskát
(2005). We used the PANTONE colour matching system
(PANTONE Formula Guide, First Edition, Third Printing, 2001. Pantone Inc., Carlstadt, New Jersey, USA.) for
identifying colours: the background colour was identified as
light sepia, somewhat similar to beige or ivory; spots were
sepia (457C) or dark brown (614C). Weight of artificial
cuckoo eggs (ca. 3.23.5 g) was adjusted to be similar to the
weight of a real cuckoo egg (2.93.8 g; Wyllie 1981). Nests
were experimentally parasitised on the day when the fourth
egg was laid by exchanging one host egg with an artificial
cuckoo egg. Nests were monitored daily after the experiment, in the period of six days, or until the parasitic egg was
ejected, or the nest was deserted. We did not use nests that
were depredated within this control period. Three types of
reactions were observed: (1) no reaction, i.e. acceptance of
the parasitic egg, (2) desertion of the nest, and (3) ejection
of the parasitic egg. The coat of the eggs was suitable to
show peck marks from the hosts if they tried to eject these
model eggs. Sometimes hosts made small holes in the
middle part of these relatively hard model eggs by pecking
them several times before ejection, as if seeking the
possibility to pierce and hold these eggs in their bills, as
video recordings revealed (Honza and Moskát 2008). In
about 25% of the cases of ejections, the attempts were not
successful and the parasitic eggs remained in the nests, but
heavy peck marks reflected to the trials of ejection (Moskát
unpubl. data). If peck marks were seen in the body of the
eggs, i.e. under the paint coat, we categorised them as
ejections. Although great reed warblers at the Apaj site
rejected different egg types in a wide range (8100%;
Moskát et al. 2008), previous studies reported fairly
consistent reactions against the egg type applied in the
present study (6571%; Moskát et al. 2002, Moskát 2005).
Site fidelity of the birds in the population was measured
by banding chicks and adults using standard colour rings,
and monitoring their return rate in subsequent years.
Statistical analyses were performed using SPSS 10.0
(SPSS Inc. 1999). We used parametric statistical tests when
a variable was normally distributed and non-parametric
tests for non-normal variables, as assessed by the ShapiroWilk test for normality (Zar 1996).
Molecular methods and analyses
We genotyped great reed warbler nestlings, one per nest (22
individuals from Apaj Channels, 19 individual from Tisza
and 18 individuals from Lake Velence) for variation at nine
microsatellite loci (G61, Aar1, Aar2, Aar4, Ase7, Ase18,
Ase34, Ase44 and Ase50; for details and primer sequences
see Hansson et al. 2000, 2004, and Richardson et al. 2000).
Previous work showed that these loci are polymorphic in
great reed warblers, with expected heterozygosity levels
ranging from 10% at locus Ase50 to 71% at locus G61 in a
Swedish population (Hansson et al. 2000, Hansson 2004).
For comparison, we also genotyped 22 individuals from
each of three populations in Sweden located 70140 km
from each other (Lake Hornborgasjön, Lake Kvismaren and
Lake Tåkern; for details of these populations see Hansson
et al. 2002a,b).
The genotyping protocol that we used has been
described in Hansson et al. (2000), and Richardson et al.
(2000), but we will repeat some of the details here. We
isolated DNA from blood samples with phenol/chloroformisoamylalcohol extraction, and the DNA samples were then
diluted to a concentration of 25 ng/ml. Microsatellite alleles
were amplified with PCR in GeneAmp 9700 thermal
cyclers (Applied Biosystems). The PCR-mix contained
4 pmol of each primer, 1NH4-buffer, 15 nmol MgCl2,
2 nmol dNTP, 0.5 U AmpliTaq Polymerase (Perkin Elmer)
and 25 ng template in 10 ml reaction volume. One of the
primers in a pair was labelled with a fluorescent dye (6FAM or HEX). PCR-conditions were as follows: 948C for 2
min, then 35 cycles at 948C for 30 s/TA for 30 s/728C for
665
30 s, followed by 728C for 10 min; where TA is the locusspecific annealing temperature (locus/TA; G61/56, Aar1/62,
Aar2/60, Aar4/53, Ase7/60, Ase18/60, Ase34/60, Ase44/
60, Ase50/60). The fluorescent-labelled PCR-products were
separated in 6% acrylamid gels and the alleles were detected
in a FluoroImager SI (Molecular Dynamics, Inc.). The
PCR products of at least two individuals with known allele
lengths were run in each gel as size standards.
Degree of population differentiation was calculated by
the program ARLEQUIN 3.1 and significance of FSTvalues was generated using 10,000 permutations (Schneider
et al. 2000).
Results
Rejection rate, genetic structure and dispersal
Great reed warblers showed similar reactions against the
model cuckoo eggs in the three study sites; they rejected the
non-mimetic parasitic eggs at high rates (71%, 82%, 76%
in the sites Apaj Channels, Tisza River and Lake Velence,
respectively; Fig. 2). None of the differences in rejection/
acceptance ratios between any pairs of populations proved
to be significant (Fisher’s exact test, two-tailed: Apaj
Channels vs Tisza River: P 0.528; Apaj Channels
vs Lake Velence: P1.0; Tisza River vs Lake Velence:
P 0.711). Great reed warblers rejected almost all model
cuckoo eggs by ejection, we observed only one nest
desertion in Apaj and another one in the Tisza site.
There was no significant genetic differentiation between
any of the three Hungarian populations (Table 1). The FSTvalues ranged between 0.009 and 0.007, with a value of
0.009 for the two most geographically separated populations, Lake Velence and Tisza River (distance 130 km).
Neither were the three Swedish populations genetically
differentiated (FST B 0.001, P ]0.57; Table 1). Thus, there
seems to be no or very little genetic structure in great reed
warblers on this scale (within 130 km in Hungary and
within 140 km in Sweden). There was however genetic
structure on the larger scale: when the populations were
pooled within countries, the Hungarian and the Swedish
populations had a significant FST (FST 0.016, P B0.001).
Also, two pairwise comparisons of populations in different
countries showed significant differentiation (Apaj vs Kvismaren: FST 0.038, P B0.001; Velence vs Kvismaren:
FST 0.022, P 0.022; the former was significant
also after accounting for multiple tests, k 15,
acrit_0.05 0.003; Table 1).
For understanding dispersal and site fidelity of young
great reed warblers we colour-ringed 284 great reed warbler
fledglings in three years of the study period at Apaj (14,
168, 102 birds in 1999, 2000 and 2001, respectively).
However, only three fledglings (ca. 1%) were observed in
the subsequent years in the natal site (ca. 30 15 km). We
also ringed 30 adult birds at Apaj, but of these birds only
two were recorded in the breeding area in the following
years (ca. 7% recovery rate), and one breeding bird was
marked in an adjacent area (ca. 10 km distance). However,
regarding the large size of our study area, we cannot exclude
the possibility that the actual return rate was somewhat
higher. These results suggest a very low level of natal and
666
Figure 2. Frequency of natural cuckoo parasitism on great reed
warbler populations in Hungary (a), and rejection rate of the host
towards non-mimetic artificial cuckoo eggs in three study sites,
‘‘Apaj Channels’’, ‘‘Tisza River’’ and ‘‘Lake Velence’’ (b). (Parasitism rate in the site ?Apaj channels? is the mean of six years:
range: 4168%. Number of nests (a) and number of experiments
(b) are shown in parentheses.)
breeding philopatry in Hungarian great reed warbler
populations.
Reproductive success
Mean clutch size of great reed warblers varied from 4.60
to 4.95 (Table 2). It did not differ between the sites Apaj
Channels and Lake Velence, in the year 2000 when
the study was carried out at both sites (Mann-Whitney,
z 1.079, P 0.281), but Apaj Channels and Tisza
River had different clutch size in the 2001 (Mann-Whitney,
z 2.538, P 0.011). No yearly fluctuations in clutch
size were revealed in Apaj Channels from 1998 to 2003
(Kruskal-Wallis ANOVA, x2 7.339, df5, P 0.197).
Reproductive success of surviving unparasitised nests, i.e.
nests that produced any output, varied between 3.58 and
4.27 fledglings/nest (Table 2). There were no significant
differences in number of fledglings neither between sites
nor between years (Apaj vs Lake Velence in the year
2000: Levene’s test: F 1.351, P 0.253; t 1.096, df 33, P 0.281; Apaj vs Tisza River in the year 2001: MannWhitney, z1.106, P0.269; Apaj, 1998 and from
Table 1. Pairwise FST values (below diagonal) from microsatellite data of three great reed warbler populations in Hungary (Apaj, Tisza and
Velence), and three Swedish populations (Hornborgasjön, Kvismaren and Tåkern) and corresponding significance values (above diagonal).
Sample sizes are given in parenthesis in the diagonal. Significance values after correcting for number of tests by the sequential Bonferroni
technique are indicated (*: PB0.05).
Apaj
Tisza
Velence
Hornborgasjön
Kvismaren
Tåkern
Apaj
Tisza
Velence
Hornborgasjön
Kvismaren
Tåkern
(22)
0.001
0.007
0.014
0.038
0.016
0.527
(19)
0.009
0.002
0.015
0.011
0.251
0.828
(18)
0.013
0.022
0.004
0.082
0.469
0.098
(22)
0.002
0.009
0.001*
0.066
0.022
0.572
(22)
0.019
0.061
0.943
0.282
0.896
0.999
(22)
2000 to 2003: Kruskal-Wallis ANOVA, x2 2.969,
df 4, P 0.563).
In the heavily parasitised population at Apaj there were
on average only 2.13 host fledglings/nest, if calculation was
based on all nests (i.e. successful unparasitised and parasitised nests). For the almost unparasitised population at
Lake Velence this value was about 3.96 fledglings/nest. So
the reproductive output of the host in the highly exploited
population was about 53.8% of the reproduction in the
almost unparasitised population. For this reason we can
regard the heavily parasitised population as lowly reproductive.
Discussion
This study revealed high similarity in rejection behaviour
and high genetic similarity of the great reed warbler
populations in Hungary, regardless of hosts being highly,
moderately, or almost not parasitised by cuckoos: (1) The
rejection rates against non-mimetic artificial cuckoo eggs
did not differ between sites. This finding suggests that hosts
in these sites are on the same level in the parasite-host
coevolutionary arms race. An earlier study showed that
some other more distantly located great reed warbler
populations differed in their response to non-mimetic
model cuckoo eggs: great reed warblers in central Greece,
possibly a former host of the cuckoo in that area, showed a
100% rejection rate, which was significantly higher than in
Hungary (71% rejection rate; Moskát et al. 2002; see a
similar example for the common redstart Phoenicurus
phoenicurus by Rutila et al. 2006). That egg discrimination
was similar in the almost non-parasitised, the moderately
parasitised, and the highly parasitised areas, suggests that
rejection behaviour is not a plastic response to the local level
of parasitism in this species. (2) No small-scale genetic
structure was found in great reed warbler, neither between
our study populations in Hungary nor between localities in
Sweden. This contrasts the results of some other passerine
species, e.g. the blue tit Cyanistes caeruleus (Foerster et al.
2006), but is in line with previous studies of the genetic
structure of the great reed warbler in Eurasia (Bensch and
Hasselquist 1999, Hansson 2003). Most European great
reed warbler populations are genetically similar to populations in neighbouring countries at neutral loci, whereas
evidences of large-scale structures exist, e.g. there are genetic
differences between western and eastern European populations (Bensch and Hasselquist 1999), northern and central
European populations (Hansson 2003, this study) and
European and Asian populations (Hansson 2003). Smallscale differences in genetically-based rejection behaviour
would arise easier if gene flow between local populations
was low. (3) The return rate of fledglings was very low in
our Hungarian populations: we observed only three recruits
in subsequent years of about 300 colour ringed fledglings.
Although Hungarian great reed warblers breed in patchy
habitats, a network of reed-vegetated channels and lakes is
available for breeding in many parts of the Hungarian Great
Table 2. Clutch size and reproductive output of surviving unparasitised nests of great reed warblers, i.e. nests that reared any fledgling, in the
three study sites in Hungary (nsample size), within the period from 1998 to 2003.
Apaj Channels
Tisza River
Lake Velence
High (4168%)
Moderate (11%)
Low (below 1%)
Parasitism rate
Eggs/nest (mean9SE)
1998
1999
2000
2001
2002
2003
4.9490.162
4.9090.143
4.9590.104
4.7090.298
4.9190.177
4.6090.149
(19)
(20)
(22)
(23)
(23)
(30)
4.6490.095 (47)
4.6890.180 (25)
Fledglings/nest (mean9SE)1
1998
2000
2001
2002
2003
4.2790.384
4.0690.234
3.9490.315
3.6790.333
3.8290.296
(11)
(17)
(17)
(12)
(11)
3.5890.253 (27)
3.6790.268 (18)
1
Year 1999 is not included because of inadequate sample size.
667
Plain and adjacent areas. Typically extensive agricultural
areas divide lakes and small networks of channels from each
other. However, these cannot be regarded as large ecological
barriers, which could have prevented dispersal of great reed
warblers and cuckoos. On the other hand, rivers and some
longer channels may function locally as dispersal corridors,
which may facilitate unifying gene flow among populations.
A conceptually similar study on reed warblers in Britain
revealed that there might be a significant population
difference in antiparasite defence (see above; Brooke et al.
1998, Lindholm and Thomas 2000). The two cases, the
Hungarian great reed warbler populations and the British
reed warblers, do however differ in several aspects. British
reed warblers breed in small and isolated marshes on the
edge of their distribution range, whereas Hungarian great
reed warblers breed in more inter-connected populations in
the central part of the breeding range (Cramp 1992). A
patchy distribution of the breeding habitats seems to
promote philopatry in other bird species, e.g. song sparrow
Melospiza melodia (Arcese 1989), savannah sparrow Passerculus sandwichensis (Wheelwright and Mauck 1998), and
Swedish great reed warblers (Hansson et al. 2002a), so a
high degree of natal philopatry may be expected in Britain,
which could have facilitated adaptation to the local level of
parasitism. The case of the magpie Pica pica, which occurs
sympatrically and allopatrically with its brood parasite, the
great spotted cuckoo, showed some similarity with our great
reed warbler populations, because extensive gene flow was
revealed between nearby populations (Martı́nez et al. 1999).
The metapopulation concept may provide a suitable
explanation to population differences in reproductive
success (Levins 1969, review in Hanski and Simberloff
1997). A good example is the red-winged blackbird Agelaius
phoeniceus, where reproductive success strongly differs
between populations due to habitat quality differences
(Vierling 2000). Brood parasitism reduces the reproductive
output of the affected host populations, so sometimes
highly parasitised population may turn into population
sinks. This was recently observed in the warbling vireo Vireo
gilvus in British Columbia, where the host suffered from
5080% rate of parasitism by the brown headed cowbird
(Ward and Smith 2000). These vireos showed no egg
discrimination ability against the brood parasite and,
although cowbird parasitism is generally not directly lethal
for nestlings, parasitised nests typically produce no vireo
young. The sink populations were maintained by immigration from unparasitised, or lowly parasitised vireo populations. Probably, high rate of cuckoo parasitism may affect
great reed warbler populations in a similar way (Barabás
et al. 2004). Without immigration, high parasitism rate
cannot be maintained over longer periods of time, because
the low reproduction of the host should lead to the
extinction of the host, and consequently extinction of the
brood parasite as well.
We conclude that great reed warbler populations in
Hungary show no genetic differentiation and also no
difference in antiparasite defence against parasitic eggs. It
is a surprising result, because parasitism rate varied locally
from about 1% to 68%. These results differ from those of
reed warblers in Britain, where populations showed
different antiparasite defence levels (cf. Brooke et al.
1998, Lindholm and Thomas 2000). We suggest that the
668
main reason for strong egg-rejection behaviour also in
unparasitised Hungarian populations is that many hosts
populations are relatively well-connected with habitat
corridors (channels) and that large dispersal barriers are
lacking, with high inter-population dispersal and gene flow
as a consequence. We also suggest that the low reproductive
success of highly parasitised populations makes these
populations vulnerable and dependent on immigration of
individuals from patches with little parasitism and high
reproductive outcome for their long-term persistence.
Acknowledgements The study was supported by the Hungarian
Scientific Research Fund (OTKA, grant No. T35015 and No.
T48397) to CM., and by the Swedish Research Council (6212005-4736) to BH. We are thankful to Tibor Kisbenedek, Marcel
Honza, József Szentpéteri, Michael I. Cherry and Péter Batáry for
their help in the fieldwork. The Duna-Ipoly National Park and the
Kiskunság National Park provided permissions for research.
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