Journal of Animal
Ecology 2007
76, 1208–1214
Individual patterns of habitat and nest-site use by hosts
promote transgenerational transmission of avian brood
parasitism status
Blackwell Publishing Ltd
JEFFREY P. HOOVER*† and MARK E. HAUBER‡
*Illinois Natural History Survey, Champaign, IL, USA; †Florida Museum of Natural History, University of Florida,
Gainesville, FL, USA; and ‡School of Biological Sciences, University of Auckland, PB 92019, Auckland, New
Zealand
Summary
1. Brood parasitic birds impose variable fitness costs upon their hosts by causing the
partial or complete loss of the hosts’ own brood. Growing evidence from multiple avian
host–parasite taxa indicates that exposure of individual hosts to parasitism is not
necessarily random and varies with habitat use, nest-site selection, age or other
phenotypic attributes. For instance, nonrandom patterns of brood parasitism had
similar evolutionary consequences to those of limited horizontal transmission of
parasites and pathogens across space and time and altered the dynamics of both
population productivity and co-evolutionary interactions of hosts and parasites.
2. We report that brood parasitism status of hosts of brown-headed cowbirds
Molothrus ater is also transmitted across generations in individually colour-banded
female prothonotary warblers Protonotaria citrea. Warbler daughters were more likely
to share their mothers’ parasitism status when showing natal philopatry at the scale of
habitat patch. Females never bred in their natal nestboxes but daughters of parasitized
mothers had shorter natal dispersal distances than daughters of nonparasitized
mothers. Daughters of parasitized mothers were more likely to use nestboxes that had
been parasitized by cowbirds in both the previous and current years.
3. Although difficult to document in avian systems, different propensities of vertical
transmission of parasitism status within host lineages will have critical implications
both for the evolution of parasite tolerance in hosts and, if found to be mediated by
lineages of parasites themselves, for the difference in virulence between such extremes as
the nestmate-tolerant and nestmate-eliminator strategies of different avian brood
parasite species.
Key-words: cowbird, habitat use, host–parasite interactions, prothonotary warbler,
virulence.
Journal of Animal Ecology (2007) 76, 1208–1214
doi: 10.1111/j.1365-2656.2007.01291.x
Introduction
Brood parasitic birds are very much like other parasites
and pathogens in that they reduce the reproductive
success of infected hosts (Ortega 1998; Davies 2000;
Hauber 2003a). Life-history theory also predicts (Forbes
& Lamey 1996; Krüger 2006) and empirical data confirm (Lyon 1998; Hauber 2003b) that the impact of
brood parasitic birds on host reproductive investment
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society
Correspondence: J. P. Hoover, Illinois Natural History
Survey, Champaign, IL, USA. Tel.: +1 618 827 4586.
E-mail: [email protected]
strategies may parallel the effects of many endo- and
ectoparasitic infestations and diseases (Martin et al.
2001). There is extensive variation in the degree of
virulence between different parasite species and across
different hosts of the same parasites (Hauber 2003b;
Kilner 2005; Grim 2006; Servedio & Hauber 2006).
Yet many hosts of avian brood parasites do not reject
parasitism by ejecting foreign eggs and chicks or
abandoning parasitized breeding attempts (Rothstein
1975). The tolerance of brood parasitism by host species
may be due to evolutionary lag (i.e. historical constraints) or may be the outcome of the higher costs of
parasite rejection strategies (e.g. recognition errors,
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Factors promoting
cowbird parasitism
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
1208–1214
physiological, ontogenetic, or cognitive constraints)
compared with the benefits of rejection (especially
when impacted by moderately virulent parasites)
(reviewed in Rothstein & Robinson 1998; Davies 1999;
Krüger 2006).
Recent theoretical work explored the implications
of how life-history trade-offs between the values of
current vs. future reproductive attempts of hosts might
contribute towards the evolution of variation both
in the extent of parasites’ virulence (Kilner 2005;
Servedio & Hauber 2006) and in the propensity of the
tolerance of parasites by hosts (Hauber, Yeh & Roberts
2004; Grim 2007). These models concur with empirical
evidence that nonrejection of brood parasitism is likely
to be observed in species where the future chance of
parasitism is nonrandomly associated with individuals’
repeated breeding attempts due to significant spatial
and temporal patterns in parasitism (i.e. limited
horizontal transmission of brood parasitism: Smith
1981; Robinson et al. 1995a; Brooker & Brooker 1996;
Grim 2002; Røskaft et al. 2002; Barabás et al. 2004;
Hoover, Yasukawa & Hauber 2006; Røskaft et al. 2006).
For example, differences in individual hosts’ parasitism
status across repeated breeding attempts are known to
vary according several ecological and phenotypic
traits, including habitat-patch use, nest-site characteristics, age, male song and parental abilities (Smith
1981; Alvarez 1993; Robinson et al. 1995b; Soler et al.
1995; Øien et al. 1996; Clotfelter 1998; Hauber &
Russo 2000; Moskat & Honza 2000; Hauber 2001;
Krüger 2004; Garamszegi & Aviles 2005; reviewed in
Parejo & Avilés 2007). Although heritable variation in
these ecological and phenotypic traits within avian
lineages is both genetically conceivable (Freeman-Gallant
& Rothstein 1999; Brown & Brown 2000; MartínGálvez et al. 2006; Serrano & Tella 2007) and theoretically critical for models of host–parasite population
dynamics and co-evolutionary interactions (May &
Robinson 1985; Barabás et al. 2004; Røskaft et al. 2006),
empirical data are still sparse and therefore much
needed from diverse host–parasite systems to explore
at the individual, population and interspecific levels
whether variation in hosts’ tolerance of avian brood
parasitism might be related to genetic lineages of hosts
experiencing spatially and temporally structured (i.e.
nonrandom) patterns of parasitism status (Røskaft
et al. 2002, 2006; Barabás et al. 2004; Krüger 2006).
Here we analyse data from long-term observations
of an extensively studied host–parasite system to
explore the ecological contexts for consistent patterns
of nonrandom parasitism status across individually
known mother and offspring hosts of a moderately
virulent avian brood parasite. Specifically, we asked the
following four questions.
1. Do mother–daughter pairs of the host species share
similar brood parasitism status of breeding attempts?
2. Do natal dispersal distances or philopatry to the
natal habitat patch affect brood parasitism status of
daughters?
3. Do patterns of nest-site use explain similarity of
mother–daughter parasitism status?
4. Are specific female host morphological traits
associated with different propensities of brood
parasitism status?
Materials and methods
To examine the possibility and the potential ecological
mechanisms of transgenerational patterns of avian
brood parasitism, we studied prothonotary warblers
Protonotaria citrea (Boddaert) and brown-headed
cowbirds Molothrus ater (Boddaert). Prothonotary
warblers are the only cavity nesting species commonly
parasitized by brown-headed cowbirds (Petit 1999;
Hoover 2003a). Prothonotary warblers are a brood
adjuster species that preferentially feed earlier hatched
and larger chicks (sensu Soler 2001) and cowbirds
hatch prior to and are larger than host chicks (Hoover
2003a). This species readily uses nestboxes for breeding
and, through researchers’ long-term monitoring of an
extensive nestbox network (established by JPH), it has
already provided a rare opportunity (Payne & Payne
1998) to explore the transgenerational consequences
of avian brood parasitism on recruitment and natal
and breeding philopatry in a small long-distance
migrant bird species (Hoover 2003b; Hoover & Reetz
2006). Our primary goals were to explore patterns
of transgenerational transmission of avian brood
parasitism status in the prothonotary warbler, a
natally philopatric acceptor host (i.e. does not reject
naturally or experimentally introduced parasite eggs)
of the moderately virulent brown-headed cowbird
(i.e. some host young survive and fledge from parasitized nests: Hoover 2003c; Kilner 2005; Grim
2006; Hoover & Reetz 2006; Servedio & Hauber
2006). We also aimed to further highlight the need for
data on host- and parasite-philopatry at the same
study sites.
To evaluate empirically the occurrence of vertical
transmission of brood parasitism status, we summarized
reproductive data collected by JPH on individually
colour-banded female prothonotary warblers breeding
in southern Illinois, USA during 1994–2006. We chose
to focus on female hosts because in species where only
females incubate, they also appear to be the rejecter
gender (Soler, Martin-Vivaldi & Perez-Contreras 2002).
For detailed methodology and description of study
sites, see Hoover (2003b, 2006) and Hoover & Reetz
(2006). Parasitism status was manipulated for many
warblers by reducing the entrance size to the nestboxes
to exclude female cowbirds’ entry (Hoover 2003a,c).
Data are included here only for female warblers whose
nests were accessible to cowbirds.
We extracted parasitism status data on individually
marked females (n = 147) that produced philopatric
daughters (n = 159, including 12 sister pairs). We
randomly chose one of the daughters for each of the 12
sister pairs and conducted our analyses using 147
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J. P. Hoover &
M. E. Hauber
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
1208–1214
unique mother–daughter pairs. Philopatric daughters
were those that bred in the study area (in any one of the
n = 1200 nestboxes spread among habitat patches
within the study area of 192 km2) during the year
subsequent to their mothers’ breeding season. There
are no multigenerational lineages in the analyses
(i.e. data from both mother–daughter, daughter–granddaughter pairs). In the absence of evidence for
intraspecific brood parasitism (i.e. nests never receive
more than one warbler egg per day; J. Hoover, personal
observations), we assumed genetic maternity between
attending females and female progeny fledged from
the same nestbox. We tested the null hypothesis that
mothers’ status of cowbird parasitism (a binary yes/no
variable) in one year was not associated with her
daughters’ status of parasitism during the progeny’s
first breeding season the next year. We documented the
location of breeding return for each daughter that was
philopatric to the study system (i.e. recruited to our
study area of 192 km2, representing approximately 10%
of banded juvenile females; Hoover & Reetz 2006). We
recorded the natal dispersal distances (distance between
the nestbox where they were produced and the nestbox
where they first bred to the nearest 5 m) of these locally
recruited daughters and whether they returned to the
habitat patch where they were produced (birth patch)
or to a different patch.
We began our analysis by exploring the totality
of our data set using a mixed-effect nominal logistic
analysis on the bivariate yes/no parasitism status of
daughters with the predictor variables of the mother’s
parasitism status (yes/no), dispersal distance (continuous data in metres), return to natal patch (yes/no), and
year (as a random effect) using JMP 5·1 (SAS Institute
Inc. 2000). We also examined if daughter–mother
similarity of parasitism status (yes/no) was related to
return to natal patch (yes/no), dispersal distance, and
year (random effect). We then conducted post-hoc
univariate and contingency analyses to explore the
directional relationships between the significant
predictor variables from the mixed-effect model.
We used a t-test to compare natal dispersal distances
between daughters from parasitized and nonparasitized mothers. Because prothonotary warblers in our
study population used fixed-site nestboxes for breeding
(Hoover 2003b), we also examined whether there was
an interannual correlation of parasitism status for the
nestboxes used by the philopatric warbler daughters.
Specifically, we used a contingency analysis to
determine if the parasitism status of a particular
nestbox used by a daughter was associated with the
status of that same nestbox in the previous year. We
employed a separate contingency analysis to test
whether daughters from parasitized mothers were
more likely than daughters from nonparasitized
mothers to use a nestbox that had been parasitized
previously.
To test the hypothesis that aspects of parasitized
female hosts’ phenotypic traits were related to the
likelihood of their nesting attempts being parasitized
by cowbirds (Lotem, Nakamura & Zahavi 1995;
Garamszegi & Aviles 2005), we used logistic regression
analyses (SAS Institute Inc. 2000) of parasitism
status and morphometric measurements of warbler
mothers and daughters (for details of how measurements were obtained, see Hoover 2003b). For these two
analyses we only included mothers (n = 129) and
daughters (n = 124) for which we had complete sets of
measurements.
The land cover in our study system changes little
from year to year and nonforest habitat surrounding
our study sites is dominated by agriculture (Hoover
2006). Breeding sites of prothonotary warblers were
located on discrete habitat patches (forested wetlands
separated from each other by > 500 m of unsuitable
breeding habitat consisting of dry forest, early successional forest or agriculture). Based on what is known
about cowbird movement patterns and habitat use in
forest ecosystems that are fragmented by agriculture
(e.g. commuting between breeding sites in forests and
feeding sites in agriculture; Thompson 1994; Gates &
Evans 1998; Thompson & Dijak 2000), we explored
the relationship between a simple land cover metric
(% forest cover within a 3-km radius of the centre of
each habitat patch) and parasitism rates on our study
sites. Per cent forest cover was determined by overlaying a 100 m grid on aerial photographs of study
sites and recording the percentage of grid points
(n = 3000) that fell on forested habitat. For this analysis we only considered the first nesting attempts
of individually marked warblers within particular
breeding season (to control for seasonal effects;
Hoover et al. 2006) that were in nestboxes accessible to
cowbirds. We determined the proportion of nests
parasitized on each of 12 habitat patches where we had
seven or more consecutive years of data (58 or more
nesting attempts per patch). We used a correlation
analysis to test the prediction that the proportion of
nests parasitized would decrease with increased
forest cover.
Results
 ‒ 
   
Our exploratory analysis using mixed-effect nominal
logistic fits revealed that daughters’ parasitism status
was only related to mothers’ parasitism status (P = 0·0003)
and not to dispersal distance (P = 0·843) or return to
natal patch (P = 0·541) in the full model (R2 = 0·12,
P = 0·012), with year included as a random effect.
With data pooled across all years, females whose own
breeding attempts were parasitized in a given year
produced daughters who were more likely to be
parasitized than predicted by chance alone based on
overall parasitism rates in the study population (χ2 =
14·254, d.f. = 1, P < 0·001, n = 147; Fig. 1a).
1211
Factors promoting
cowbird parasitism
Fig. 2. Cowbird parasitism decreased with increased forest
cover around habitat patches. Each point represents parasitism
rates for a particular habitat patch.
Fig. 1. Daughters of parasitized mothers were more likely to
be parasitized than daughters of nonparasitized mothers (a),
and daughters returning to the habitat patch where they were
produced were more likely to have the same parasitism status
as their mother than daughters returning to a different site (b).
Numbers inside bars represent sample sizes.
   
  
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
1208–1214
Daughters (n = 147) never bred in the territory where
they were produced, and therefore never used the same
nestboxes as their mothers. The vast majority (83%) of
daughters known to have returned did so to within
3 km of their natal nestbox and 55% bred within the
same habitat patch where they were produced (natal
patch). The mean (± 1 SE) natal dispersal distance for
daughters of parasitized mothers tended to be less than
daughters of nonparasitized mothers (1670 ± 192 m
vs. 2515 ± 350 m, respectively) and the difference was
nearly significant (two-tailed t = 1·901, d.f. = 145, P =
0·059). The mixed-effect analysis showed that similarity
in parasitism status between mothers and daughters was
related to daughters’ return to the natal patch (P =
0·0009), but not to dispersal distance per se (P = 0·49),
with year included as a random effect in the full model
(R2 = 0·12, P = 0·014). Daughters that returned to
breed in their birth patch were more likely to have the
same parasitism status as their mother than daughters
that returned to a different habitat patch within the study
system (χ2 = 11·208, d.f. = 1, P = 0·001, n = 147; Fig. 1b).
The proportion of nests parasitized on study sites
decreased with increased forest cover within a 3-km
radius of each site (r = 0·86, d.f. = 11, P < 0·001; Fig. 2).
    
The parasitism status of nestboxes used by daughters
was highly correlated between years. Nestboxes parasitized
Fig. 3. Parasitism status of nestboxes used by daughters was
highly correlated between years (a), and daughters of parasitized
mothers were more likely to use previously parasitized nestboxes
than daughters of nonparasitized mothers (b). Numbers
inside bars represent sample sizes.
in one year (the year prior to use by a daughter) were
usually parasitized again the next year, whereas nonparasitized nestboxes were not (χ2 = 37·252, d.f. = 1,
P < 0·001, n = 97; Fig. 3a). Daughters of parasitized
mothers were more likely to use a nestbox that had
been parasitized the previous year than were daughters
of nonparasitized mothers (χ2 = 7·406, d.f. = 1, P =
0·007, n = 97; Fig. 3b).
    

We identified no phenotypic measurements of female
prothonotary warblers’ morphology that were significant predictors of parasitism status for mothers or
daughters (Table 1).
1212
J. P. Hoover &
M. E. Hauber
Table 1. Results of logistic regression analysis of morphological traits and parasitism status of warbler mothers (n = 129)
and daughters (n = 124). P-values are based on Wald X2
score statistics
P-value
Trait
Mothers
Daughters
Wing length
Tarsus length
Mass
Mass/tarsus length
Full model
0·447
0·205
0·231
0·240
0·157
0·667
0·218
0·212
0·227
0·262
Discussion
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
1208–1214
Prior modelling and empirical studies suggest that
spatially and temporally structured patterns of avian
brood parasitism impact host co-evolution by decreasing the likelihood that antiparasite resistance strategies
spread through otherwise nonresistant host populations (Grim 2002; Røskaft et al. 2002, 2006; Brockhurst
et al. 2003; Barabás et al. 2004; Hauber et al. 2004;
Hoover et al. 2006; but see van Baalen & Jansen 2001).
Specifically, nonrandom exposure of individual
hosts to parasitism can reduce the fitness benefits of
antiparasite rejecter strategies of vulnerable hosts and,
thus, promote the persistence of nonrejecter lineages
within parasitized host populations in different brood
parasitic species through increased evolutionary lag of
the spread of rejecter antiparasite strategies (Røskaft
et al. 2002; Barabás et al. 2004; Hauber et al. 2004;
Hoover et al. 2006). In support of this possibility, our
observations on the occurrence of disproportionate
exposure of mother–daughter pairs of prothonotary
warblers to parasitism by brown-headed cowbirds
are in agreement with the hypothesis that (1) brood
parasitism status is transmitted vertically within female
host lineages.
Within the framework of life-history theory,
transgenerational transmission of avian brood
parasitism status has similar selective consequences to
the impacts of vertical transmission of infection status
by various parasites and pathogens from mothers to
progeny (reviewed in Galvani 2003). However, the
transmission of brood parasitism status within host
lineages reported here is not equivalent to the full
concept of vertical transmission whereby parasite and
pathogen lineages themselves are transmitted between
host parent and progeny, which in turn predicts the
evolution of less virulent parasites (Bull 1994; Day
2003). Nevertheless, the reported transgenerational
patterns of repeatable parasitism status are a critical
precursor of and set the stage for the evolution of
vertical transmission (Bull 1994; Galvani 2003) of avian
brood parasitism, which remains yet to be explored
empirically in any avian host–brood parasite systems.
Vertical transmission of brood parasitism is theoretically
feasible especially for those avian parasites that (1)
themselves are territorial and show natal and breeding
philopatry, and that use (2) territorial hosts that also
show natal and breeding philopatry (Sorenson &
Payne 2002; Hauber & Dearborn 2003).
The ecological correlates of individuals’ exposure to
cowbird parasitism of prothonotary warblers reported
in this study imply that the mechanism of vertical
transmission of parasitism status is related to shared
breeding habitat use by mother–offspring pairs of
hosts. Remarkably, this pattern arose in the absence of
any nestboxes being reused by daughters following
breeding by their mothers contrary to predictions of
the hypothesis that (2a) daughters return to breed in
natal nesting cavities (Semel & Sherman 2001). Instead,
interannual parasitism risk on nesting attempts in this
host population appears to be closely associated with
habitat traits, including proportional forest coverage
within close proximity to discrete habitat patches
(Fig. 2). Accordingly, philopatry to the natal habitat
patch was strongly correlated with whether warbler
daughters ‘inherited’ the parasitism status of their
mothers: daughters returning to the same habitat patch
where they were produced in the previous year were
more likely to share the same parasitism status with
their mothers. These patterns are consistent with the
hypothesis that (2b) females return to the location of
their natal habitat patch (e.g. natal philopatry: Weatherhead & Forbes 1994). In particular, daughters of
parasitized mothers had shorter natal dispersal
distances than daughters of nonparasitized mothers,
leading to a disproportionate parasitism rate of daughters
of parasitized mothers (Fig. 1a). Consistent parent–
offspring similarity of habitat and nest-site use has also
been described in some other avian systems (Thorpe
1945; Brown & Brown 2000; Serrano & Tella 2007).
At the microhabitat scale, individual nest sites had
consistent interannual patterns of parasitism status
(also see Hauber 2001; Hoover et al. 2006). Again,
daughters did not use their natal nestboxes, but our
data supported the hypothesis that (3) daughters were
more likely to nest in boxes that also shared the parasitism
status of their mothers in the previous year. This implies
a similar choice, and apparent heritability, for a particular
parental trait (Freeman-Gallant & Rothstein 1999)
by mothers and daughters in the use of nesting sites and
breeding territories, mediated by either genetic or maternal
effects (Brown & Brown 2000) or learning through
nest-site and habitat imprinting (Thorpe 1945).
Finally, because our data are correlative with regards
to warblers’ parasitism status, we cannot exclude the
hypothesis that (4) shared phenotypic traits of parents
and offspring caused the transmission of parasitism status
across years (Garamszegi & Aviles 2005). None the less,
even though our measures did not specifically address
explicit aspects of the quality of parasitized vs. nonparasitized individuals (Soler et al. 1995; Parejo & Aviles
2007), contrary to this scenario we found no morphological
traits of daughters or mothers (also see Hoover et al.
2006) that were strong predictors of parasitism status.
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Factors promoting
cowbird parasitism
Why is there a spatio-temporal structure to parasitism
in cowbird-host systems? Our findings of spatially consistent patterns of cowbird parasitism status of natally
philopatric daughters at the habitat-patch scale (hypothesis 2 above) are consistent with the complementary
hypothesis that (5) host parasitism status across years
are due to consistency in both habitat configurations and
cowbird behaviours across years (Robinson et al. 1995a,b;
Hoover, Tear & Baltz 2006). In support, brown-headed
cowbirds use habitat in a predictable manner by commuting between feeding and breeding sites on a daily basis
(Rothstein, Verner & Stevens 1984; Thompson 1994;
Robinson et al. 1995b; Thompson & Dijak 2000).
Taken together with previous work on limited
horizontal transmission of brood parasitism due to the
spatio-temporal structure of parasitism risk experienced by individual hosts (Hauber et al. 2004;
Hoover et al. 2006), our results have consequences for
the co-evolutionary dynamics of hosts and parasites.
Transgenerational transmission of brood parasitism
status affects the variation both in the reproductive
outputs of consistently parasitized over nonparasitized
host lineages and in the relative fitness benefits of hosts’
resistance strategies over acceptor strategies. Furthermore, given the extensive variation in avian brood
parasite virulence (Kilner, Madden & Hauber 2004;
Kilner 2005; Grim 2006), we specifically predict that
vertical transmission of avian brood parasitism should
be prevalent in evolutionary lineages of nonrejecter
hosts of nestmate-tolerant parasites.
Acknowledgements
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
1208–1214
This paper is dedicated to the late Professor Jamie N.
M. Smith. For discussions and comments we are
grateful to A. Galvani, M. Goddard, T. Grim, R. Kilner,
A. Lotem, C. Moskat, J. Parra, R. Payne, S. Robinson,
H. Ross, J. Smith, B. Strausberger, C. Tonra,
K.Yasukawa, and many other colleagues. Comments
provided by three anonymous reviewers also improved
the manuscript. The drawings were prepared by V.
Ward. We thank the numerous field assistants who
helped collect warbler data over several years. Financial
support was provided by the United States Fish and
Wildlife Service (INT 1448-0003-95-1007), The Nature
Conservancy, the Illinois Department of Natural
Resources Wildlife Preservation Fund, The National
Fish and Wildlife Fund, the University of Illinois
(Dissertation Completion Fellowship and Travel Grant),
the North American Bluebird Society, the Champaign
County and Decatur Audubon Societies, and Sigma Xi
(to JPH); and the National Geographic Society, the
New Zealand Marsden Fund, the Human Frontier
Science Program, and the University of Auckland
Research Council (to MEH). Any opinions, findings
and conclusions or recommendations expressed in
this publication are those of the authors and do not
necessarily reflect the views of the agencies and
organizations that supported the research.
References
Alvarez, F. (1993) Proximity of trees facilitates parasitism by
cuckoos Cuculus canorus on rufous warblers Cercotrichas
galactotes. Ibis, 135, 331.
van Baalen, M. & Jansen, V.A.A. (2001) Dangerous liaisons:
the ecology of private interest and common good. Oikos,
95, 211–224.
Barabás, L., Gilicze, B., Takasu, F. & Moskát, C. (2004)
Survival and anti-parasite defense in a host metapopulation
under heavy brood parasitism: a source-sink dynamic
model. Journal of Ethology, 22, 143 –151.
Brockhurst, M.A., Morgan, A.D., Rainey, P.B. & Buckling,
A. (2003) Population mixing accelerates coevolution.
Ecology Letters, 6, 975–979.
Brooker, M.G. & Brooker, L.C. (1996) Acceptance by the
splendid fairy-wren of parasitism by Horsfield’s bronzecuckoo: further evidence for evolutionary equilibrium in
brood parasitism. Behavioral Ecology, 7, 395–407.
Brown, C.R. & Brown, M.B. (2000) Heritable basis for choice
of group size in a colonial bird. Proceedings of the National
Academy of Sciences USA, 97, 14825 –14830.
Bull, J.J. (1994) Virulence. Evolution, 48, 1423 –1435.
Clotfelter, E.D. (1998) What cues do brown-headed cowbirds
use to locate red-winged blackbird host nests? Animal
Behaviour, 55, 1181–1189.
Davies, N.B. (1999) Cuckoos and cowbirds versus hosts:
coevolutionary lag and equilibrium. Ostrich, 70, 71–79.
Davies, N.B. (2000) Cuckoos, Cowbirds, and Other Cheats.
T&AD Poyser, London.
Day, T. (2003) Virulence evolution and the timing of disease lifehistory events. Trends in Ecology and Evolution, 18, 113–118.
Forbes, L.S. & Lamey, T.C. (1996) Insurance, developmental
accidents, and the risk of putting all your eggs in one basket.
Journal of Theoretical Biology, 180, 247–256.
Freeman-Gallant, C.R. & Rothstein, M.D. (1999) Apparent
heritability of parental care in Savannah Sparrows. Auk,
116, 1132–1136.
Galvani, A. (2003) Epidemiology meets evolutionary biology.
Trends in Ecology and Evolution, 18, 132–139.
Garamszegi, L.Z. & Aviles, J.M. (2005) Brood parasitism by
brown-headed cowbirds and the expression of sexual
characters in their hosts. Oecologia, 143, 167–177.
Gates, J.E. & Evans, D.R. (1998) Cowbirds breeding in the
central Appalachians: spatial and temporal patterns and
habitat selection. Ecological Applications, 8, 27–40.
Grim, T. (2002) Why is mimicry in cuckoo eggs sometimes so
poor? Journal of Avian Biology, 33, 302–305.
Grim, T. (2006) Low virulence of brood parasitic chicks: adaptation or constraint? Ornithological Science, 5, 237–242.
Grim, T. (2007) Experimental evidence for chick discrimination
without recognition in a brood parasite host. Proceedings
of the Royal Society of London B, 274, 373 – 381.
Hauber, M.E. (2001) Site selection and repeatability in
brown-headed cowbird (Molothrus ater) parasitism of
eastern phoebe (Sayornis phoebe) nests. Canadian Journal
of Zoology, 79, 1518 –1523.
Hauber, M.E. (2003a) Hatching asynchrony, nestling competition, and the cost of interspecific brood parasitism.
Behavioral Ecology, 14, 227–235.
Hauber, M.E. (2003b) Interspecific brood parasitism and the
evolution of host clutch sizes. Evolutionary Ecology
Research, 5, 559–570.
Hauber, M.E. & Dearborn, D.C. (2003) Parentage without
parental care: what to look for in genetic studies of obligate
brood-parasitic mating systems. Auk, 120, 1–13.
Hauber, M.E. & Russo, S.A. (2000) Perch proximity correlates with higher rates of cowbird parasitism of ground
nesting song sparrows. Wilson Bulletin, 112, 150–153.
Hauber, M.E., Yeh, P.J. & Roberts, J.O.L. (2004) Patterns and
coevolutionary consequences of repeated brood parasitism.
1214
J. P. Hoover &
M. E. Hauber
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
1208–1214
Proceedings of the Royal Society of London B, 271, S317–
S320.
Hoover, J.P. (2003a) Multiple effects of brood parasitism
reduce the reproductive success of prothonotary warblers,
Protonotaria citrea. Animal Behaviour, 65, 923 –934.
Hoover, J.P. (2003b) Decision rules for site fidelity in a migratory bird, the prothonotary warbler. Ecology, 84, 416–430.
Hoover, J.P. (2003c) Experiments and observations of prothonotary warblers indicate a lack of adaptive responses to
brood parasitism. Animal Behaviour, 65, 935 –944.
Hoover, J.P. (2006) Water depth influences nest predation for
a wetland-dependent bird in fragmented bottomland
forests. Biological Conservation, 127, 37– 45.
Hoover, J.P. & Reetz, M.J. (2006) Brood parasitism increases
provisioning rate, and reduces offspring recruitment and adult
return rates, in a cowbird host. Oecologia, 149, 165–173.
Hoover, J.P., Tear, T.H. & Baltz, M.E. (2006) Edge effects reduce
the nesting success of acadian flycatchers in a moderately
fragmented forest. Journal of Field Ornithology, 77, 425– 436.
Hoover, J.P., Yasukawa, K. & Hauber, M.E. (2006) Spatially
and temporally structured avian brood parasitism affects
the fitness benefits of hosts’ rejection strategies. Animal
Behaviour, 72, 881– 890.
Kilner, R.M. (2005) The evolution of virulence in brood
parasites. Ornithological Science, 4, 55 – 64.
Kilner, R.M., Madden, J.R. & Hauber, M.E. (2004) Brood
parasitic cowbird nestlings use host young to procure
resources. Science, 305, 877– 879.
Krüger, O. (2004) Breeding biology of the cape bulbul Pycnonotus capensis: a 40-year comparison. Ostrich, 75, 211–216.
Krüger, O. (2006) Cuckoos, cowbirds and host: adaptations,
trade-offs and constraints. Philosophical Transactions of
the Royal Society of London Series B, 361, doi: 10.1098/
rstb.2006.1849.
Lotem, A., Nakamura, H. & Zahavi, A. (1995) Constraints on
egg descrimination and cuckoo-host co-evolution. Animal
Behaviour, 49, 1185–1209.
Lyon, B.E. (1998) Optimal clutch size and conspecific brood
parasitism. Nature, 392, 380–383.
Martin, T.E., Moller, A.P., Merino. S. & Clobert, J. (2001)
Does clutch size evolve in response to parasites and
immunocompetence? Proceedings of the National Academy
of Sciences USA, 98, 2071–2076.
Martín-Gálvez, D., Soler, J.J., Martínez, J.G., Krupa, A.P.,
Richard, M., Soler, M., Møller, A.P. & Burke, T. (2006) A
quantitative trait locus for recognition of foreign eggs in the
host of a brood parasite. Journal of Evolutionary Biology,
19, 543 –550.
May, R.M. & Robinson, S.K. (1985) Population dynamics of
avian brood parasitism. American Naturalist, 126, 475– 494.
Moskat, C. & Honza, M. (2000) Effect of nest and nest site
characteristics on the risk of cuckoo Cuculus canorus parasitism in the great reed warbler Acrocephalus arundinaceus.
Ecography, 23, 335–341.
Øien, I.J., Honza, M., Moksnes, A. & Røskaft, E. (1996) The
risk of parasitism in relation to the distance from reed
warbler nests to cuckoo perches. Journal of Animal Ecology,
65, 147–153.
Ortega, C.P. (1998) Cowbirds and Other Brood Parasites.
University of Arizona Press, Tucson, AZ.
Parejo, D. & Avilés, J.M. (2007) Do avian brood parasites
eavesdrop on heterospecific sexual signals revealing host quality? A review of the evidence. Animal Cognition, 10, 81–88.
Payne, R.B. & Payne, L.L. (1998) Brood parasitism by cowbirds:
risks and effects on reproductive success and survival in
indigo buntings. Behavioral Ecology, 9, 64 –73.
Petit, L.J. (1999) Prothonotary warbler, Protonotaria citrea.
The Birds of North America (eds A. Poole & F. Gill), no. 408.
Birds of North America, Philadelphia, PA.
Robinson, S.K., Thompson, F.R. III, Donovan, T.M.,
Whitehead, D.R. & Faaborg, J. (1995a) Regional forest
fragmentation and the nesting success of migratory birds.
Science, 267, 1987–1990.
Robinson, S.K., Rothstein, S.I., Brittingham, M.C., Petit, L.J.
& Grzybowski, J.A. (1995b) Ecology and behavior of cowbirds and their impact on host populations. Ecology and
Management of Neotropical Migratory Birds (eds T.E.
Martin & D.M. Finch), pp. 428 – 460. Oxford University
Press, New York.
Røskaft, E., Moksnes, A., Stokke, B.G., Moskát, C. &
Honza, M. (2002) The spatial habitat structure of host
populations explains the pattern of rejection behavior in
hosts and parasitic adaptations in cuckoos. Behavioral
Ecology, 13, 163 –168.
Røskaft, E., Takasu, F., Moksnes, A. & Stokke, B.G. (2006)
Importance of spatial habitat structure on establishment of
host defenses against brood parasitism. Behavioral Ecology,
17, 700–708.
Rothstein, S.I. (1975) An experimental and teleonomic investigation of avian brood parasitism. Condor, 77, 250–271.
Rothstein, S.I. & Robinson, S.K. (1998) Parasitic Birds and
Their Hosts, Studies in Coevolution. Oxford University
Press, New York.
Rothstein, S.I., Verner, J. & Stevens, E. (1984) Radio-tracking
confirms a unique diurnal pattern of spatial occurrence in
the parasitic brown-headed cowbird. Ecology, 65, 77–88.
Semel, B. & Sherman, P.W. (2001) Intraspecific parasitism and
nest-site competition in wood ducks. Animal Behaviour, 61,
787–803.
Serrano, D. & Tella, J.L. (2007) The role of despotism and
heritability in determining settlement patterns in the
colonial lesser kestrel. American Naturalist, 169, E53–E67.
Servedio, M.R. & Hauber, M.E. (2006) To eject or to abandon? Life history traits of hosts and parasites interact to
influence the fitness payoffs of alternative anti-parasite
strategies. Journal of Evolutionary Biology, 19, 1585–1594.
Smith, J.N.M. (1981) Cowbird parasitism, host fitness, and
age of the host female in an island song sparrow population.
Condor, 83, 152–161.
Soler, M. (2001) Begging behaviour of nestlings and food
delivery by parents: the importance of breeding strategy.
Acta Ethologica, 4, 59–63.
Soler, J.J., Soler, M., Møller, A.P. & Martinez, J.G. (1995)
Does the great spotted cuckoo choose magpie hosts
according to their parenting ability? Behavioral Ecology
Sociobiology, 36, 201–206.
Soler, M., Martin-Vivaldi, M. & Perez-Contreras, T. (2002)
Identification of the sex responsible for recognition and the
method of ejection of parasitic eggs in some potential
common cuckoo hosts. Ethology, 108, 1093–1101.
Sorenson, M.D. & Payne, R.B. (2002) Molecular genetic
perspectives on avian brood parasitism. Integrative and
Comparative Biology, 42, 388 – 400.
SAS Institute Inc. (2000) SYSTAT, Version 10·0. SPSS Science,
Chicago, IL.
Thompson, F.R., III (1994) Temporal and spatial patterns of
breeding brown-headed cowbirds in the midwestern United
States. Auk, 111, 979–990.
Thompson, F.R., III & Dijak, W.D. (2000) Differences in
movements, home range, and habitat preferences of female
brown-headed cowbirds in three midwestern landscapes.
Ecology and Management of Cowbirds and Their Hosts (eds
J.N.M. Smith, T.L. Cook, S.I. Rothstein, S.K. Robinson & S.G.
Sealy), pp. 100 –109. University of Texas Press, Austin, TX.
Thorpe, W.H. (1945) The evolutionary significance of habitat
selection. Journal of Animal Ecology, 14, 67–70.
Weatherhead, P.J. & Forbes, M.R.L. (1994) Natal philopatry
in passerine birds: genetic or ecological influences? Behavioral Ecology, 5, 426 – 433.
Received 18 October 2006; accepted 3 July 2007
Handling Editor: Robert Poulin