Behavioral Ecology Vol. 13 No. 2: 163-168
© 2002 International Society for Behavioral Ecology
The spatial habitat structure of host populations explains the pattern of rejection behavior in hosts and parasitic adaptations in cuckoos
a Department of Zoology, Norwegian University of Science and Technology, NTNU, N-7491 Trondheim, Norway b Animal Ecology Research Group of the Hungarian Academy of Sciences, c/o Hungarian Natural History Museum, H-1083 Budapest, Ludovika ter 2, Hungary c Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Kvetná 8, 60365 Brno, Czech Republic
Address correspondence to E. Røskaft. E-mail: roskaft{at}chembio.ntnu.no .
Received 14 November 2000; revised 24 March 2001; accepted 24 March 2001.
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ABSTRACT |
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In this article we present tentative support for predictions derived from a spatial habitat structure hypothesis arguing that common cuckoos Cuculus canorus, the most common obligate brood parasite in Europe, only breed in areas where they have access to vantage points in trees. Thus, species in which some populations breed near trees while other populations breed farther from trees have a different cuckoo—host population dynamic than species in which all populations always breed in the vicinity of trees. Parasitism rate, mimicry of brood parasite eggs with those of the hosts, and rejection behavior of hosts varies with the host breeding habitat. Cuckoos are best adapted to exploit species in which some populations breed near trees while other populations breed in open areas because such hosts are not always accessible to cuckoos, and thus gene flow among unparasitized and parasitized populations delays the evolution of host adaptations. Adaptive behavior in cuckoos as well as in their hosts can be predicted from the spatial habitat structure hypothesis.
Key words: brood parasitism, cuckoos, Cuculus canorus, gene flow, habitat structure, host behavior, metapopulation.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Theoretical analyses have shown that the spatial structure of populations may strongly influence their evolutionary processes, and analyses of host—parasite models have shown that patterns of gene flow among different local populations affect their ability to counteract the parasitism (Gandon et al., 1996
;
Grenfell and Harward, 1997;
Schlichting and Pigliucci,
1998; Via et al.,
1995). Thus local microadaptations may affect the behavioral
traits of different populations breeding in a metapopulation system.
In the Old World, the common cuckoo Cuculus canorus is an obligate
brood parasite that lays its eggs in the nests of a variety of host species,
mainly smaller passerines. As the cuckoo dramatically reduces the hosts'
breeding success (Øien et al.,
1998; Røskaft and
Moksnes, 1998), there should be strong selection for the evolution
of counteradaptations by the hosts. Many investigations have shown that
mechanisms of egg recognition have evolved among the hosts to counteract brood
parasitism (Brooke and Davies,
1988; Davies and Brooke,
1988;
1989a,
b; Moksnes et al.,
1990,
1991). Such egg recognition
behavior by the hosts has led to selection for host-egg mimicry by the cuckoo
(Baker, 1942; Davies and
Brooke, 1989a,
b;
Lack, 1968;
Moksnes and Røskaft,
1995).
It is reasonable to assume that the success of brood parasites will vary
both temporally and spatially according to different environmental factors
such as habitat structures and densities of host populations. It could be
adaptive for hosts to modify their responses to parasitism according to
variation in these factors (Øien et
al., 1999). Experimentally parasitized hosts of the cuckoo are
known to reject the foreign egg more frequently when they have seen a female
cuckoo near the nest (Davies and Brooke,
1988; Moksnes et al.,
1993b). The rejection rates of cuckoo hosts also vary with the
degree of similarity between the parasite's and the host's egg
(Brooke and Davies, 1988;
Davies and Brooke, 1988).
Furthermore, phenotypic plasticity may occur: individuals that either ejected
or accepted a cuckoo egg in a first test frequently change their response in
subsequent tests (e.g., rufous bush robin Cercotrichas galactotes;
Soler et al., 2000). Because
the parasitism pressure of brood parasites may vary spatially as well as
temporarily, it has recently been stressed that host responses toward cuckoo
parasitism have to be regarded in a metapopulation perspective
(Lindholm, 1999;
Lindholm and Thomas,
2000).
Many host populations show intermediate reactions toward the cuckoo egg, as
both rejection and acceptance occurs
(Davies and Brooke, 1989a;
Moksnes et al., 1990). Such
populations may be at an equilibrium between individuals that accept and
individuals that reject, as a compromise between the cost of parasitism and
the cost of recognition errors (Lotem et al.,
1992,
1995; Takasu,
1998a,
b;
Takasu et al., 1993;
Rodriguez-Gironés and Lotem,
1999). Recently a new hypothesis explaining the coexistence of
acceptors and rejecters in the same host population (the intermittent arms
race hypothesis; Soler et al.,
1998) has been suggested. This hypothesis is based on the
existence of spatially structured, cyclic changes in parasitism over many
years, where the host population will respond to the variation in parasitism
pressure.
Although the equilibrium hypothesis may explain the intermediate rejection
rates in some populations, it does not explain the dynamics of metapopulations
nor the plasticity different host populations show in their responses toward
cuckoo eggs (Lindholm, 1999;
Lindholm and Thomas, 2000).
Furthermore, the equilibrium hypothesis cannot predict the level of acceptance
rate of different host species. Unparasitized host populations of several
brood parasite species may accept almost all parasitic eggs experimentally
laid in their nests (Davies and Brooke,
1989b; Soler and
Møller, 1990; Lindholm
and Thomas, 2000). Interpopulation variation has been attributed
to phenotypic plasticity, but it may as well be genetically determined and due
to differences in gene flow between acceptor and rejecter populations. The
degree of mimicry of cuckoo eggs with those of the hosts may also vary among
populations (Moksnes and Røskaft,
1995).
In this article we argue that the interpopulation variation in rejection
behavior within a species is determined by gene flow between unparasitized and
parasitized populations. Differences in rejection rates of cuckoo eggs will
affect the degree of host egg mimicry as well as the rate of parasitism. We
have made some important prerequisites for this approach. First, in many
potential host species some populations are heavily parasitized by cuckoos,
whereas others are not parasitized at all
(Davies and Brooke, 1989b).
The metapopulation approach assumes that unparasitized populations are sources
for parasitized ones because, everything else being equal (e.g., predation
pressure), the average fitness will be lower in parasitized populations, which
will lead to vacancies and immigration of recruits from unparasitized
populations. Thus gene flow from the sources where there is no selection for
egg rejection to the sinks, where there is selection for rejection, leads to a
dimorphic response in the sink populations. In parasitized populations the
cuckoos will evolve mimetic eggs to lower the rate of egg rejection. Second,
because cuckoos are dependent on trees (or in recent time, electrical poles or
wires) as vantage points for finding host nests
(Alvarez, 1993;
Øien et al., 1996;
Moskát and Honza,
2000), host populations breeding in the vicinity of trees will be
more exposed to parasitism than host populations breeding farther from trees.
Thus, there will be a difference between species that always breed near trees
and those breeding both near and far from trees, with some populations being
exposed to cuckoo parasitism while others are not.
From this spatial habitat structure hypothesis, we develop the following
predictions: (1) in species where all populations always breed near trees, the
host should rapidly evolve rejection behavior, and the cuckoo should only
occasionally match the speed of this evolution and only sporadically develop
matching mimetic eggs. Thus, in habitats with trees, suitable hosts should
always be good rejecters (
100%), whereas cuckoo egg morphs matching those
of the hosts will be rare. Parasitism rate should be low. (2) Among species
breeding in habitats where some populations are breeding close to trees where
they are heavily parasitized by cuckoos, whereas others are breeding far from
trees where they are unparasitized, gene flow among populations should delay
the evolution of rejection behavior in parasitized populations. If the
frequency of unparasitized populations is high, the result should be a high
variation in rejection behavior among populations. Cuckoos should evolve egg
mimicry in parasitized populations. We expect the average mimicry of cuckoo
eggs to be better among these species than among species always breeding near
trees. (3) Host species that always breed in open areas far from trees should
be acceptors, even though they in theory are suitable hosts. There should be
no selection for egg mimicry, and parasitism rate should always be very low
(no data exist, however, to test this prediction).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In this study we collected data from different sources. In the analyses we have used data on 24 different European cuckoo hosts because available data on their rejection rates of non-mimetic cuckoo eggs exists (Table 1; see below). Only suitable hosts are included in this analysis. Suitable hosts are defined as having nests that are accessible for the cuckoo. They feed their chicks with food that is digestible for the cuckoo chick, and they have a nest size and egg size that make it possible for the young cuckoo to eject the nest contents (Davies and Brooke, 1989a
;
Moksnes et al., 1990).
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Rejection rates of different host species toward nonmimetic cuckoo eggs
were collected from published papers or from own unpublished experiments in
Norway, Hungary, and the Czech Republic
(Alvarez, 1999;
Brooke et al., 1998;
Brown et al., 1990;
Davies and Brooke, 1989a;
Gärtner, 1982;
Järvinen, 1984;
Moskát and Fuisz, 1999;
Moksnes and Røskaft,
1992; Moksnes et al.,
1990,
1994;
Stokke et al., 1999;
von Haartman, 1981). A hosts'
rejection rate is defined as the proportion of eggs that was rejected (ejected
or deserted) of the total number of experiments with artificial, nonmimetic
cuckoo eggs added to the clutch. Experiments from different populations were
pooled (Table 1).
Three breeding habitats were identified. The first type is always near
trees (13 species; Table 1),
where cuckoos in principal always have access to all host nests due to the
proximity of trees (Figure 1).
Second, some populations (near trees) are accessible to cuckoos, while others
(far from trees) are not (seven species). Some host species such as the
redstart Phoenicurus phoenicurus, robin Erithacus rubecula,
pied wagtail Motacilla alba, and wren Troglodytes
troglodytes are partly hole nesters or breed in cavities in some areas
and are therefore inaccessible to cuckoos. They are included in this group.
Altogether 11 species are therefore included in this group
(Table 1). A third category of
species always breeds far from trees
(Figure 1); however, it is not
included in this analysis because no data exist. We used the criteria of Snow
and Perrins (1998) to
determine the breeding habitats and nest sites of the different species. For
simplicity we used only two habitats in the analyses (always near trees; near
and far from trees).
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The frequency of matching egg morphs of the different species was taken
from a study of more than 12,000 cuckoo eggs in European museums
(Moksnes and Røskaft,
1995). A matching cuckoo egg morph is a cuckoo egg that is said to
be similar to the eggs of the host (e.g., a blue cuckoo egg similar to the
blue eggs of the redstart; Moksnes et al.,
1995). Fourteen species have a matching cuckoo egg morph; 10
species have no matching cuckoo egg morph
(Table 1). The information
regarding the matching egg morph of the rufous bush robin has been taken from
Alvarez (1994).
We also used the mean degree of cuckoo egg mimicry from the museum
collections. For each parasitized clutch we scored the mimicry of the cuckoo
egg with the host eggs according to a scale from 1 to 5, where 1 is perfect
mimicry, 2 is good mimicry, 3 is medium mimicry, 4 is poor mimicry, and 5 is
maximum contrast (Moksnes and
Røskaft, 1995; Table
1).
Rate of parasitism was obtained by using data from published papers
averaged over the actual range (Davies and
Brooke, 1989b; Glue and
Murray, 1984; Lack,
1963; Moksnes and
Røskaft, 1987; Moksnes
et al., 1993b; Moskát
and Honza, 2000; Schulze-Hagen
et al., 1996; Wasenius,
1936; Wyllie,
1981). In addition, we used a number of nests containing cuckoo
eggs found in European museums (Moksnes
and Røskaft, 1995). Because, in general, data on parasitism
rates are poor, we used only two categories of parasitism rate: 1, normally
parasitized at a rate less than 1%, and 2, normally parasitized up to 5%, but
frequently even higher (Table
1).
Treating each species as an independent data point may lead to
overestimating the true number of degrees of freedom in statistical analyses
(Felsenstein, 1985;
Harvey and Pagel, 1991). To
control for possible effects of common descent, the species used in the
analysis were organized in a phylogenetic tree. We produced one tree based on
molecular data (DNA hybridization; Sibley
and Ahlquist, 1990) and another based upon morphology
(Howard and Moore, 1991). In
the latter tree, we assumed polytomies between species within a genus, between
genera within a family, and so on. To obtain a normal distribution, the
rejection rate had to be arcsin transformed before the analysis. We used the
computer program package PDAP (Phenotypic Diversity Analysis Programs; Garland
et al., 1993,
1999) version 5.0 to make the
tree and to load variable data. This package also contains Felsenstein's
(1985) independent comparison
method, which allowed us to obtain paired contrasts of the variables between
nodes in the phylogenetic trees that were independent of each other. The
branch lengths were assigned by the method of Grafen
(1989), by the method of Pagel
(1992), or set as a constant
(= 1). The branch length assignments that were used varied for each trait and
also among the trees. We selected the branch lengths that yielded absolute
values of contrasts that were not related to their standard deviations
(p <.05) for any of the traits analyzed
(Garland et al., 1992). The
relationship between the variables was analyzed by multivariate General Linear
Models (GLM). All the tests are two-tailed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The mean rejection rate was 78.3% (± 25.1, SD) for species always breeding near trees, and it was 45.6% (± 27.6, SD) for species breeding near trees as well as farther away from trees, a difference which proved to be statistically significant (arcsin-transformed data, ANOVA, F1,23 = 9.21, p =.006). The percentage of species that normally were parasitized at a rate > 1% was much higher for species breeding in both kinds of habitats (100% of the species), whereas 10 of 13 species always breeding near trees (76.9%) were normally parasitized at a rate < 1% (Fisher's Exact probabilities test, p =.000). The mean degree of mimicry of the cuckoo eggs toward those of the hosts was 3.6 (± 0.7, SD) for species always breeding near trees and 3.0 (± 0.5, SD) for species breeding in both kinds of habitats, a significant difference (ANOVA, F1,23 = 4.94, p =.037; the mean of one species was used as a unit). Finally, the percentage of species with a matching cuckoo egg morph differed significantly between species always breeding near trees and those breeding both near and far from trees. A cuckoo egg morph similar to the eggs of the host was found among 90.9% of the species breeding in both habitats, but it was found among only 30.8% of the species always breeding near trees (Fisher's Exact probabilities test, p =.005).
A multivariate GLM test using habitat as the independent variable and
(arcsin) rejection rate, whether a species was frequently parasitized > 1%
or not, and the degree of mimicry of the cuckoo eggs as dependent variables
proved to be statistically significant (Wilks's 
,
F3,21 = 11.9, p =.000). All the dependent
variables were statistically significant (arcsin rejection rate, p
=.006; parasitism rate, p =.000; degree of mimicry, p
=.037). Multivariate GLM tests based on phylogenetically independent contrasts
obtained from trees based on DNA hybridization or morphology, where habitat
was the independent variable and where rejection rate, parasitism rate, and
egg mimicry were dependent variables also proved to be statistically
significant (DNA hybridization, Wilks's , F3,21 =
8.34, p =.001; morphology, Wilks's ,
F3,21 = 6.92, p =.002). In most cases the
dependent variables were statistically significant (arcsin rejection rate: DNA
hybridization, p =.026; morphology, p =.013; parasitism
rate: DNA hybridization, p =.000; morphology, p =.000,
degree of mimicry: DNA hybridization p =.033), except for degree of
mimicry in the test based on morphology (p =.247).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Our results tentatively support the spatial habitat structure hypothesis. The breeding habitat of the host species explains their rejection behavior, the rate of parasitism by the cuckoo, and whether or not the cuckoo has developed a mimetic egg morph. The differences between species always breeding near trees or those breeding both near and far from trees were always in the direction of the predictions derived from the hypothesis. Thus, we have shown that important adaptations in both the cuckoos and their hosts can be explained by the spatial structure of habitats among breeding populations, even when controlling for phylogeny of different hosts.
Although the equilibrium hypothesis (Lotem et al.,
1992,
1995; Takasu,
1998a,b;
Takasu et al., 1993;
Rodríguez-Gironés and Lotem,
1999) may explain the level of rejection in relation to parasitism
rate of many species, it does not predict which species should be parasitized
or which species should have the highest level of rejection. However, the
spatial habitat structure hypothesis does explain the variation between
different species with regard to egg mimicry, as well as rejection and
parasitism rates. The support for the spatial habitat structure hypothesis
also gives strong support to the arms race hypothesis
(Davies and Brooke, 1989b;
Moksnes et al., 1990).
The puzzle of why so many European hosts (and hosts of other brood
parasites; Brooker et al.,
1990; Rothstein,
1990) have intermediate rejection rates has interested scientists
for a long time. Recently the variation in rejection rates between host
populations has been considered to be a result of phenotypic plasticity
(Brooke et al., 1998;
Lindholm, 1999) or conditional
host strategies (Øien et al.,
1999). These alternatives are, however, not mutually exclusive to
the spatial habitat structure hypothesis because plasticity in antiparasite
behavior may be higher for species in which parasitism pressure is variable
(e.g., among species breeding both near and far from trees).
In this study we used only a bimodal model, including two types of
habitats. However, the metapopulation system is dynamic, and we may regard a
host species as representing a system where both the proportion of populations
breeding near trees and the parasitism rate of populations vary from 0 to 100%
(Figure 2). One prediction that
can be derived from the spatial habitat structure hypothesis is that there
should be a close relationship between the proportion of populations that
breed near trees and the total rejection rate of the species
(Figure 2). Species where about
50% of the populations breed near trees and 50% breed away from trees should
have intermediate rejection rates. Species that always breed far from trees
should be acceptors. Hole-nesting birds are not accessible to cuckoos,
although a few individuals that do not breed in holes may successfully rear
young cuckoos. Hole nesters should therefore behave as if they were breeding
in more or less open habitats. Some of the European larks (Alaudidae) breed
far from trees, and they are rarely parasitized by cuckoos
(Moksnes and Røskaft,
1995), although they in principle may be suitable hosts. We
therefore predict that these larks would be acceptors.
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Species that in principle always breed near trees should be close to 100%
rejecters. The definition of a tree is critical for this hypothesis, but it
should be of a size that makes it easy for the cuckoo to use as a vantage
point (> 3-4 m high). The density of trees should be so high that cuckoos
can use alternative vantage points. Cuckoos probably prefer to use vantage
points giving them an overview of several host nests at a time
(Clarke et al., 2001). Dense
forests are probably not good cuckoo habitats because dense vegetation will
make it difficult for the cuckoo to observe host nests. Therefore, open
forests or areas with scattered trees would be the best areas for cuckoos to
use as vantage points. Normally hosts are more exposed when breeding near
trees (Alvarez, 1993;
Øien et al., 1996;
Moskát and Honza,
2000). For species breeding in such habitats, the rejection rate
will quickly evolve to a high level, making it difficult for the cuckoo to
successfully parasitize them. Therefore, parasitism rates should be highest
for species breeding both near trees as well as far from trees
(Figure 2). This explains why
species like some of the Acrocephalus warblers may be locally
parasitized at frequencies up to 15% or more
(Molnár, 1944;
Moksnes et al., 1993b;
Moskát and Honza, 2000;
Schulze-Hagen et al., 1996;
Øien et al., 1999).
Mimicry of the cuckoo egg toward those of the hosts should be best among the
species where about 50% of the populations breed among trees.
However, none of the European species is always parasitized, even among species always breeding near trees. Among such species, some populations may escape parasitism by the cuckoo, although it would be hard to conclude whether this is a result of antiparasite behavior of hosts or of cuckoos preferring other hosts because the density of the most suitable hosts is too low. This phenomenon may explain why none or very few of the European host species has a 100% rejection rate.
Data on one of the tested hosts do not support the spatial habitat
structure hypothesis. The dunnock Prunella modularis, a species that
always breeds near trees, has in previous studies been found to be an
exception to the patterns of other European hosts
(Davies and Brooke, 1989b;
Moksnes et al., 1990).
Understanding why the dunnock is such an exception has been difficult.
However, we suggest that one should look closer into their habitat and whether
this species in some populations breeds in dense forests, in cavities, in very
low densities, or if this species has not evolved antiparasite adaptations due
to a time lag (Rothstein,
1982,
1990).
We conclude that the spatial habitat structure hypothesis explains the pattern of rejection behavior in hosts and parasitic adaptations in cuckoos in Europe. This conclusion can be drawn despite the fact that the quality of data used in the present analyses is not optimal because rejection rates, parasitism rates, and degree of mimicry are not only taken from different host populations but often from populations far apart. In further research we recommend that researchers collect data on rejection rates, parasitism rates, cuckoo egg mimicry, and even dispersal rates of adult and juvenile birds from both parasitized and unparasitized populations in areas that are not too far from each other (50-100 km).
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ACKNOWLEDGEMENTS |
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We thank the Norwegian Research Council for providing funds for this project and the staff in different national and natural history museums for their assistance. We thank Jon Swenson and Bernt-Erik Sæther for constructive comments on an earlier version of this manuscript.
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