Behavioral Ecology Vol. 13 No. 4: 487-496
© 2002 International Society for Behavioral Ecology
Facultative development of courtship and communication in juvenile male cowbirds (Molothrus ater)
Department of Psychology, Indiana University, Bloomington, IN 47405, USA
Address correspondence to M.J. West, Department of Psychology, Indiana University, 1101 E. 10th St., Bloomington, IN 47405, USA. E-mail mewest{at}indiana.edu .
Received 14 December 2000; revised 22 August 2001; accepted 5 October 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We investigated effects of naturally occurring variation in experience with adult males on development of song and courtship competence in captive juvenile cowbirds. We studied birds in groups housed in large outdoor aviaries that allowed birds to regulate access to social stimulation. In two aviaries, we housed juvenile males and females either with or without adult males. Birds remained in these conditions from September 1999 through their breeding season. We documented social and vocal development of juvenile males in the two aviaries by measuring social assortment and patterns and frequencies of their song interactions. We then brought the juveniles from the two aviaries together to compete against each other for access to females. In addition, we recorded juveniles' songs four times over the study and played back their breeding season songs to females in sound-attenuating chambers to measure the effectiveness of songs in eliciting copulatory responses from the females. Compared to juvenile males housed with adult males, juvenile males housed without adult males developed atypical behavior patterns. They (1) displayed little intrasexual aggression or near-neighbor associations and (2) exhibited different patterns of courtship and copulation, but (3) were as successful at competing for copulations. Furthermore, they developed stereotyped songs sooner and developed more potent breeding season songs. These different outcomes could not be traced to one variable but to a cascade of effects involving diverging patterns of song acquisition and social interaction. The patterns of social skills that emerged indicate considerable plasticity in the mechanisms underlying acquisition of courtship competence.
Key words: cowbirds, developmental ecology, facultative development, Molothrus ater, social behavior, social learning.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The social environment is a component of an animal's ecology that can have extensive effects on development. For many animals, interactions with conspecifics are predictable and stable sources of information and selection throughout life (Heyes and Galef, 1996
; Mousseau and Fox,
1998; West-Eberhard,
1983). The social world in which an animal develops can provide
opportunities for learning about food, habitat, mates, and communication
(Doligez et al., 1999;
Freeberg, 1998;
Galef, 1996;
Nordby et al., 2000;
Stamps and Krishnan, 1999;
ten Cate and Bateson, 1988;
West and King, 1988).
Within a social environment, variation in densities and assortments of
peers, mates, and relatives can change the environmental landscape
dramatically, and with it the costs and benefits of interacting with others.
Social environments are created from a number of individuals with differing
interests, strategies, and experience where information may flow through only
subsections of populations or at different rates
(Dolman et al., 1996;
Mottley and Giraldeau, 2000;
Reader and Laland, 2000).
The brown-headed cowbird (Molothrus ater) is as an excellent model
to explore how social environments can organize and control behavioral
development because the species experiences such a wide variation in social
ecology. Being brood parasites, cowbirds spend their early life unexposed to
species-typical behavior, but once they fledge, they join cowbird flocks that
can vary extensively in age and sex composition
(Friedmann, 1929). Because
cowbirds have been so successful in expanding their range, they can now be
found in a variety of different physical and social ecologies. Cowbirds
inhabit most parts of North America (Smith
et al., 2000,Smith et al.,
2000), and they have been reported to parasitize many different
species (more than 200 different host species;
Rothstein and Robinson, 1998)
in almost any type of habitat (Morrison et
al., 1999). Across their range, cowbirds can experience
differences in population density
(Johnsgard, 1997), climate
(Ortega, 1998), sex ratio
(Rothstein et al., 1986;
Woolfenden et al., 2001), and
timing of the breeding season (Ortega,
1998). Different groups show regional differences in song dialects
and whistles (King and West,
1988; Rothstein et al.,
1988); some populations migrate, and some do not
(Ortega, 1998). Adults and
juveniles may migrate different distances
(Cristol et al., 1999).
Variation also exists in their mating systems, which can range from
promiscuity with no pair bonds to polygyny, polyandry, and monogamy, which
seems to be most prevalent (Barnard,
1998; Rothstein et al.,
1986).
Thus, cowbirds can experience myriad different social environments. In some
locations, throughout their first year juveniles may never interact with
adults, whereas in other locations juveniles join flocks of other cowbirds
while adults are still in the final days of breeding and remain with them for
the entire year (Friedmann,
1929; O'Loghlen and Rothstein,
1993; Rothstein et al.,
1980). Flocks composed of all females, all juveniles, and all
classes have been reported in the field
(Friedmann, 1929). Such
diversity in ecology and behavior provided us the impetus to study how young
cowbirds come to behave in ways appropriate to their group. We focused on what
can be learned within these social groups by juvenile males in their first
year; a time in which they must learn to sing, interact with others in their
group, and court and mate in the breeding season.
Past work has shown that social learning is important for juvenile cowbirds
to develop normally. For example, male song is influenced by interactions with
females and other males (O'Loghlen and
Rothstein, 1993; West and
King, 1988). Furthermore, development of courtship competence and
even mate preferences are influenced by exposure to conspecifics
(Freeberg, 1998;
Freeberg et al., 1995;
West et al., 1996). These
studies, however, have not directly focused on what young males can learn from
about males. In many other species of songbirds, adult males are the important
source of learning for young males. For example, song sparrows (Melospiza
melodia) learn songs from hearing adult males in the vicinity
(Beecher, 1996). In cowbirds,
however, at least regarding learning about song, it is not clear what role
adult males play. Juvenile male cowbirds have the ability to copy songs from
adult males (King and West,
1989), but they can also develop species-typical song without
exposure to adults (King and West,
1977).
Some research provides evidence that juvenile male cowbirds do indeed
acquire information important for successful reproduction from adult males. In
a recent study, Smith et al.
(2002) placed a group of 75
cowbirds composed of both sexes and of juvenile and adult age classes in a
large aviary system and observed their social interactions for a year.
Throughout the year, birds assorted based on similarity in age and sex.
However, juvenile males that associated more with adult males were more
successful in courting females than were juvenile males that associated less
with adult males. Because these effects were found in one group, however, the
causative nature of these associations could not be determined.
The current study was undertaken to investigate the importance of the
presence or absence of adult males in the social environment on juvenile male
development. In large aviaries, we housed groups of juvenile males with
females and either with or without adult males. Therefore, for half of the
juvenile males, the social group contained both age classes of males and for
the other half, adult males were absent. We wanted to study not only how
juveniles learn song, but also how they learn to use song to negotiate their
social environment (West et al., in
press). We thus observed juveniles' social behavior within the
groups over the course of their first year, focusing on the development of
singing interactions. For cowbirds, song is the critical component of the
communication system. It is used in male—male counter-singing bouts to
establish dominance hierarchies in a group
(Dufty, 1986) and singing
persistently to females is required to mate successfully.
A main goal of our work was to study social learning and development in a
group setting that provided the animals opportunities to self-select
information to be learned. An animal must acquire species-typical behavior
while dealing with the social pressures of group living and possible
competition for informational resources. Although laboratory studies have
amply documented the potential interaction between social interaction and
vocal learning, many such studies provide animals with information in largely
compartmentalized settings where the information for learning is restricted by
choices made by the experimenter. In such contexts, the learner may not be
able to regulate access to information (e.g., when caged tutors or tape
recordings are used). In addition, the animal may be spared knowledge of the
natural efficacy of using newly acquired vocal or social skills because the
relevant social contingencies do not exist in the captive setting. Studies of
song learning in birds that are sensitive to the self-regulated nature of
social contexts have begun to produce novel insights into how social
experience can affect opportunities for learning and development
(Beecher et al., 1994;
Bell et al., 1998;
Kroodsma et al., 2000; Nordby
et al., 1999,
2000;
Payne and Payne, 1993;
Petrinovich, 1988).
For these reasons we studied juvenile male development in large aviaries
where we attempted to remove experimenter-imposed barriers between social and
vocal learning by maintaining an environment with species-typical sources of
information and species-typical feedback. Although the aviaries were large,
they obviously cannot be considered directly analogous to natural conditions.
The social compositions of the groups, however (i.e., social groups with adult
males present or social groups with adult males absent) do occur naturally and
are comparably stable in the wild (King
and West, 1988).
We were interested in both the breeding season outcomes of the effect of adult males on juveniles and the processes that led to these outcomes. We thus observed birds throughout the experiment and measured social behavior in each condition to track the developmental trajectories of communicative and courtship abilities of the juveniles. Over the fall, winter, and spring before the breeding season, we recorded near-neighbor associations of all the birds to provide a measure of the overall social environment and to determine where opportunities for learning existed. We also measured social interactions by conducting a census of song production and song use for all the males in the conditions. For outcome measures we observed males' courtship success in the breeding season in both their home aviary and then in a new aviary where juveniles from the two conditions could compete against each other for copulations with new females. We also recorded songs of males in each season and analyzed song structure. Finally, we played males' breeding season songs to females in sound-attenuating chambers to measure the effectiveness of the songs in eliciting females' copulatory postures.
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METHODS |
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Subjects
We collected 20 juvenile male, 10 juvenile female, 5 adult male, and 14 adult female brown-headed cowbirds in Monroe County, Indiana, USA, to serve as subjects throughout the experiment. We determined juveniles to be between 50 and 70 days of age by plumage and date of capture. Adult birds were at least 1 year old at the beginning of the experiment. We trapped birds in July and August of 1999 in three areas; two areas were on the laboratory property within 0.25 km of each other and one was located on a horse farm approximately 15 km southwest of the laboratory. Because it was impossible to know much about the prior experiences of the birds being trapped, we randomly assigned birds to conditions ensuring that location and date of capture of the individuals was randomized. We found no systematic differences in behavioral outcomes of individuals based on trapping location or date of capture. We marked all birds with uniquely colored leg bands to permit individual identification. We housed birds in two large 9.1 x 21.4 x 3.4 m outdoor aviaries, where we provided them daily with vitamin-treated water and white millet, red millet, and canary seed plus a modified Bronx zoo diet for blackbirds. The two aviaries were visually and acoustically isolated from each other. Ecological conditions in the two aviaries were similar, with each containing trees, perches, feeding stations, and a grass-covered ground surface and shelters. Being outdoors, birds were exposed to weather conditions, wild local cowbirds that would occasionally land on the aviaries, and the attention of predators.
The only difference between the two aviaries was the presence or absence of adult males. We randomly assigned birds to the two aviaries in the following numbers. In both aviaries, we housed seven adult and five juvenile females. In one aviary, referred to as the juvenile male—adult male condition (JA), we housed eight juvenile males and five adult males. In the second aviary, referred to as the juvenile male condition (J), we housed 12 juvenile males and no adult males. Density and sex ratio were the same between conditions. All birds remained in their home aviaries from September 1999 through June 2000. Across the entire year, two juvenile males, one adult male, and one adult female died in the JA condition and one juvenile female and one adult female died in the J condition.
Procedure
For 404 total observation hours from September through June, two observers
recorded birds' vocal behavior (using song censuses; see below) and social
assortment behavior (using near-neighbor associations; see below) for 0.5 to
1.5 h per aviary, starting between 0600 h and 0800 h, depending on seasonal
variation in sunrise, and ranging from 5 to 7 days per week. We divided
observations into two phases: prebreeding season (22 September through 27
April) and breeding season (28 April through 1 June). At the end of the
breeding season phase, we removed birds from their home aviaries and conducted
a mating competency tournament, combining subsets of juvenile males from the
two conditions in a new aviary with a new group of females.
Song censuses consisted of 15-min blocks in which observers occasion-sampled aviaries, noting any male that vocalized. For each vocalization, we recorded whether it was directed toward another bird or was undirected. To be scored as a directed vocalization, the bird had to vocalize toward a recipient, oriented on axis between approximately 0° and 45°. The distance between vocalizing bird and recipient could not exceed 60 cm. We considered vocalizations produced that were not oriented to another bird as undirected. We recorded a soliloquy from any bird that made 10 consecutive, undirected vocalizations within approximately 1 min. Once a bird sang a soliloquy, we did not record any more undirected vocalizations from him for the duration of the census block.
Using 7-min sampling blocks, we recorded near-neighbor associations by sampling each bird (referred to as the "target") in an aviary and noting any other bird (referred to as the "near neighbor") that was within 30 cm. Once we recorded a pair as near neighbors, they could not be recounted as another near-neighbor association unless the pair moved apart and then reassociated. Inter-observer reliability for the prebreeding season was high for song census measures of songs per male and for near neighbor associations per bird (both r =.89, both p <.001).
For the first 8 months, we manually recorded measures on data sheets.
During the breeding season, we developed and began using a system for
automated data collection using voice recognition
(White et al.,
2002,White et al.,
2002). We used IBM ViaVoice Millennium Pro Edition voice
recognition software operating on a Pentium III, 500 MHz IBM-compatible
computer (Compaq Deskpro EP), running Microsoft Windows 98. We used a
solid-state, wireless, omni-directional lapel microphone (Telex WT 150; Telex
Communications Ltd.) and receiver system (Telex FMR 150). Microsoft Word 2000
word processing software transcribed speech into text. We then exported text
into a database (4th Dimension v. 6.5.1; ACI Inc.) that we
programmed to match incoming text to a list of possible codes to detect and
correct errors automatically. Interobserver reliability was high using voice
recognition for song censuses (songs per male; r =.98, p
<.001) and for near-neighbor associations (near-neighbor associations per
bird; r =.87, p <.005).
Prebreeding season
We divided the prebreeding season into three samples: fall (22 September
through 27 November), winter (10 January through 1 March), and spring (2 March
through 27 April). The amount of observation time in each sample was equal at
37.5 h per condition for song censuses and 9.33 h for nearneighbor measures.
At the end of each sample, we calculated for each juvenile the number of
soliloquies sung and the number of vocalizations directed to males
(male-directed song) and females (female-directed song). Also, to measure the
length of singing interactions, defined as any instance where a male sang at
least one directed song to an individual recipient, we calculated mean songs
per interaction as the average number of vocalizations a male directed to an
individual recipient within a song census block.
Breeding season
The breeding-season phase commenced on the day of the first observed
copulation and continued until we began removing birds from home aviaries for
the mating competency tournament. We observed birds between 0600 and 1000 h,
the time when virtually all copulations occur
(Rothstein et al., 1986). We
continued to measure near-neighbor associations as we did in the prebreeding
season for a total of 35 observation hours. The implementation of voice
recognition for song censuses allowed us to record new behaviors in addition
to singing. We recorded a "leave" when the recipient of a directed
vocalization flew away within 1 s of the end of the vocalization. We recorded
a "depart" when a bird that made a directed vocalization flew away
from the recipient within 1 s of the end of the vocalization. Leaves and
departs were thus measures of disruptions of singing interactions. We recorded
all "copulations," defined as a male mounting a female that had
assumed a copulatory posture. We defined a "copulatory posture" as
a female arching her back in response to a directed vocalization. We recorded
"usurps," occurring when males attempted to copulate with females
that had gone into a posture as a result of another male's vocalization.
Finally, we scored "fights" when males came into physical contact
with one another. We conducted 75.75 observation hours of song censuses in the
breeding season.
Mating competency
To compare courtship abilities of juveniles from the two conditions, we
conducted a mating competency tournament. We combined a random selection of
three juveniles from each condition in a new test aviary, identical to their
home aviaries, and observed their courtship success with a group of three
juvenile and four adult females that had formerly been housed in an aviary
with adult males. We observed birds each morning from 0600 h to 1000 h for a
total of 42.25 observation hours. We used song censuses procedurally identical
to the breeding season censuses. To test the possibility that scan sampling
vocalizing males was systematically biasing our observations, we also took
15-min focal samples on each male in the competition each day, recording the
same measures as in song censuses. During these focal samples, we continued to
scan for and record any copulations that occurred in the aviary. Focal and
scan sampling measures produced similar patterns of results for singing
(r =.72, p <.001). We collected 3.16 times more data in
scan samples than we did in focal samples.
We considered a male a success in the tournament if he copulated more than
three times or consorted with the same female for 3 days in a row. We
considered a male to have obtained a consort day with a female if he either
copulated with her or sang the majority of his female-directed songs to her.
The consort persistence measure (3 consecutive consort days with the same
female) has been shown in the past to be a predictor of copulatory success
(Freeberg et al., 1995). We
considered males failures if they sang less than one female-directed song per
day over a 4-day period. When males reached criterion for success or failure,
we replaced them with males from their original conditions. The test continued
until all males from one condition competed in the tournament.
Song recordings
We recorded juvenile males' vocalizations in fall (October 1999), winter
(December 1999), spring (April 2000), and finally when their vocalizations had
crystallized in the breeding season (May 2000). We made the recordings in
their home aviaries using Sennheiser RF condenser microphones recorded into a
Sony TCD-D10 PRO digital audiotape recorder. To measure the rate of
development and quality of the songs of juvenile males, we (1) documented the
emergence of mature song elements in each bird's vocal repertoire from the
recording sessions before the breeding season and (2) played the breeding
season recordings to females in sound attenuating chambers, measuring each
song's efficacy in eliciting a copulatory response from the females.
Song development
We measured the rate of development of song for each juvenile in the two
conditions by tracking the emergence of note clusters within their
vocalizations. Note clusters are typical features of mature crystallized
cowbird song. We plotted songs on a zero-crossing oscilloscope and printed
them to paper. Samples averaged approximately 30 vocalizations per male from
the fall recording, 20 vocalizations per male in winter, 20 vocalizations per
male in spring, and 50 vocalizations per male in the breeding season. For any
vocalization to be regarded as a note cluster, we had to be able to detect at
least two notes ranging from 300 Hz to 1400 Hz (low-voice notes) and two notes
ranging from 1500 Hz to 13000 Hz (high-voice notes). Low- and high-voice notes
had to alternate within the note cluster, and all four had to be represented
within approximately 200 ms. For each recording session, we then determined
the proportion of each male's vocalizations that could be classified as note
clusters.
Playbacks
We dubbed the breeding season recordings selected for playback onto an
Otari MX III half-track recorded at 36 cm/s. We played back songs using an
Otari recorder, a Urei 537 1/3-octave equalizer, and a Crown D75 power
amplifier through JBL 2105 speakers located in each sound-attenuating chamber.
The sound pressure levels of the songs were 85 ± 2 dB (a weighted
impulse reading at 0.8 m from the speaker as recorded by a B&K 2209 sound
pressure meter). We selected one song from each male in the two conditions
based on recording quality from a selection of approximately 50 songs per
male. Signal-to-noise ratios, measuring peak noise to peak signal, did not
differ between songs from the JA and J conditions (means 48.84 and 48.87,
respectively, Student's t test, t14 = 0.028,
ns).
Starting on 15 May 2000, we played the songs to a group of females composed
of eight adults and six juveniles that had previously been housed in an
outdoor aviary from September 1999. The females had been housed without males
in the aviary, but they could see, hear, and interact through the aviary wire
with resident cowbirds. On 27 April 2000, we brought the females into the lab
and housed them in pairs in 1.3-m3 chambers. Housing females in
pairs reduced potential stress from being housed in chambers and has been
shown to have no influence on females' responses to played back song
(Smith et al.,
2000,Smith et al.,
2000; West et al.,
1996). We played six songs per day to females. Each song trial was
separated by 90 min. We alternated the order in which we played back songs,
with each presented six times over the course of the experiment. We scored a
positive response if the female adopted a copulatory posture within 1 s from
the onset of the song. To calculate potencies, we computed mean number of
responses per female for each song and averaged over all males in each
condition. We removed one adult female from the experiment who never responded
to any playbacks.
Statistical analysis
We considered the fall, winter, and spring phases of the prebreeding season
as three separate experiments for statistical purposes. Due to small sample
sizes and heterogeneity of variance between conditions, we used nonparametric
statistical analyses throughout. For illustrative purposes, however, we depict
means, standard errors, and ranges in results.
We found no significant differences between juvenile and adult females between or within conditions for any measures across the study. We thus combined classes of females in analyses.
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RESULTS |
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Prebreeding season
Singing
Juvenile males in the two conditions displayed different vocal and social patterns throughout the months before the breeding season. Figures 1,2,3,4 depict male singing (mean songs per male) for the three seasons. J-condition juvenile males sang significantly more soliloquies (Figure 1) in the fall (Mann-Whitney U test, U5,12 = 14, p <.05), winter (U = 8, p <.01), and spring (U = 3, p <.001) than did JA-condition juvenile males. J juveniles sang fewer female-directed songs (Figure 3) than did JA juveniles in winter (U = 4, p <.005) and had similar trends in the fall (U = 17.5, p >.08) and spring (U = 15, p >.052). J juveniles also sang significantly fewer male-directed songs than did JA juveniles during each season (all U < 13, all p <.05; Figure 2). JA juveniles sang 64% (± 0.09) of their male-directed songs to juvenile males (juvenile male-directed song) during the fall, 49% (± 0.06) during the winter, and 37% (± 0.07) during the spring. There was no significant difference between conditions comparing juvenile male-directed song (all U> 20). J juveniles had fewer songs per interaction across all seasons (all U < 1.5, all p <.001; Figure 4), even when only comparing songs per interaction for juvenile male-directed song (all U < 5, all p <.005). Within the JA condition, juvenile males sang significantly more songs per interaction with adult males than with juvenile males in winter (3.26 ± 0.45 songs per interaction vs. 2.40 ± 0.20, respectively; Wilcoxon T test, T6 = 0, p <.05) and spring (2.84 ± 0.45 vs. 1.99 ± 0.26; T6 = 0, p <.05) but not fall (2.24 ± 0.27 vs. 2.11 ± 0.25; T6 = 9, ns).
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Near neighbor
Between the two conditions, there were large, significant differences in
juvenile male near-neighbor associations. Compared to J juvenile males, JA
juvenile males had significantly more near-neighbor associations with other
juvenile males in the fall (U7,12 = 0, p
<.001), winter (U6,12 = 0, p <.001), and
spring (U6,12 = 0, p <.001;
Figure 5). JA juveniles also
had significantly more near-neighbor associations with females in the fall
(U7,12 = 0, p <.001) and winter
(U6,12 = 0, p <.001) but not spring
(U6,12 = 20, ns; Figure
6) than did J juveniles.
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Adult males
Singing patterns of adult males in the JA condition were variable among
males and across seasons before the breeding season. In fall, adult males sang
(mean songs per adult male) 17.5 (± 4.11) soliloquies, 113.25 (±
34.87) male-directed songs (31% [± 0.05] of which were juvenile
male-directed), 19.25 (± 11.45) female-directed songs, and 1.95
(± 0.22) songs per interaction. In winter, adult males sang 24
(± 9.74) soliloquies, 163 (± 99.23) male-directed songs (65%
[± 0.10] of which were juvenile male-directed), 16.75 (± 11.67)
female-directed songs, and 2.31 (± 0.57) songs per interaction. In
spring, adult males increased singing to 21 (± 3.54) soliloquies, 964.5
(± 105.79) male-directed songs (41% [± 0.20] of which were
juvenile male-directed), 185.75 (± 55.17) female-directed songs, and
2.43 (± 0.22) songs per interaction.
Summary
Juvenile males differing only in exposure to adult males displayed
dramatically different patterns of singing and social assortment from early in
fall to late spring. J juvenile males engaged in more noninteractive,
undirected singing and engaged in less interactive, directed singing. When
they did sing to other birds, J juveniles sang fewer songs per interaction
than did JA juvenile males. Furthermore, as measured by near-neighbor
associations, J juveniles spent less time in close association with other
birds. We continued observing juveniles in their home aviaries into the
breeding season to determine whether these patterns of behavior from the
prebreeding season revealed differences that were important to development of
courtship behavior.
Breeding season
A summary of singing performance is depicted in
Table 1. There were no
significant differences in amount of song produced by juveniles between
conditions. Differences in how the birds used their song, however, did exist.
As a proportion of the number of directed songs sung, J juvenile males had
more leaves in response to directed song (U = 1, p <.01)
and more departs (U = 10, p <.02). There was also a
significant difference in how juveniles in the two conditions distributed
female-directed song. JA juveniles sang 82.7% of their female-directed songs
to their consort female (the female to whom the male sang the most of his
female-directed song), whereas J juveniles distributed more female-directed
song to other females, singing a significantly smaller proportion to their
consort (54.8%; U = 4, p <.005).
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A summary of courtship performance is depicted in Table 2. There were no significant differences in courtship abilities between the two conditions as measured by copulations and postures (U = 33, ns). There were, however, significant differences in other breeding-related measures. Only J juveniles ever engaged in usurps (U = 3, p <.001). J juveniles were less aggressive than JA juveniles as measured by total fights (U = 0.5, p <.001) and by fights among juvenile males only (U = 11.5, p <.01). The majority of females that copulated in the J condition copulated with more than one partner (6/9 females, mean of 2.11 partners), whereas no females in the JA condition ever copulated with any male other than their consort (Fisher's Exact test, p <.01).
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Figure 7 depicts near-neighbor associations for the breeding season. JA juveniles engaged in more near-neighbor associations with other juvenile males than did J juveniles (U6,12 = 2, p <.001). There was no difference in associations among juvenile males and females between the two conditions (U6,12 = 27, ns).
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Summary
Juvenile males housed with adults displayed singing and courtship patterns
typical of juvenile males raised in an environment with all classes of birds
(Smith et al., 2002) and
typical of behavior reported in the field
(Rothstein et al., 1986).
Juvenile males housed without adult males, however, exhibited a pattern of
courtship behavior heretofore undescribed for cowbirds in Indiana. These males
engaged in few extended bouts of singing, displayed little intrasexual
aggression, did not consort consistently with individual females, and
copulated with several females. Differences also existed across conditions in
the behavior of females. Females in the J condition copulated with several
partners, whereas females in the JA condition each copulated with one
male.
Although we suggested here that both groups of juveniles were equally successful at getting copulations, it could be argued that the comparison of courtship abilities across conditions was not appropriate because JA juveniles were competing against adult males. We therefore conducted the mating-competence tournament to compare the courtship abilities of the two classes of juveniles.
Mating competency
Table 3 presents a summary
of juvenile male singing and courtship for both conditions. Three of the six
JA juvenile males tested reached criterion for success and six out of eight J
juvenile males tested reached criterion for success (Fisher's Exact test, ns).
Of those who sang to females, J juveniles sang fewer directed songs to females
but received significantly more copulations per female-directed song than did
the JA juveniles (U6,6 = 5, p <.05).
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Summary
J juvenile males were successful in courting a new group of females when
placed in direct competition with JA juveniles. In fact, the significant
difference in number of copulations received per female-directed song and the
trends in number of birds reaching success, number of days to reach success,
number of copulations, and number of consort days all suggest that the J
juveniles were more successful in the competition than the JA juveniles.
Song analysis
Song development
Over the entire set of recordings, we documented 11 note clusters that were
sung repeatedly between J juvenile males and 13 repeatable note clusters for
JA juveniles. Compared to JA juveniles, J juvenile males had a significantly
greater proportion of vocalizations that were classified as note clusters in
fall (0.22 of JA juvenile vocalizations and 0.70 of J juvenile vocalizations;
U12,5 = 2, p <.002) and in spring (0.96 and
0.99, respectively; U12,6 = 11.5, p <.02) and
had a similar trend in winter (0.59 and 0.76, respectively;
U12,5 = 12, p >.058). For reference, 93% of
vocalizations of adult males in the JA aviary were classified as note clusters
in fall, and 100% in spring. Adults did not vocalize enough in winter to
record a representative sample. In addition, J juveniles had a significantly
higher proportion of their spring songs match exactly their song types sung in
the breeding season than did JA juveniles (0.45 of spring vocalizations
compared to 0.19, respectively, U12,6 = 6, p
<.005). There was also a difference in the structure of the songs. A
cowbird song is typically sung with two note clusters but can be sung with
three. Significantly more J juveniles (11/12) had three-note cluster songs in
their breeding season song repertoires than did JA juveniles (0/6; Fisher's
Exact test, p <.001). We recorded no three-note cluster songs from
adult males in the JA condition.
Playbacks
Females responded with a copulatory response significantly more often to
the songs of J juveniles than they did to songs of JA juveniles (Wilcoxon
T test, T13 = 91, p <.001;
Figure 8).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The presence of adult males in the juvenile males' social environment had significant influences on the development of juveniles' vocal and courtship behaviors. Compared with juvenile males housed without adults, juvenile males that had experience interacting with adult males (1) engaged in more and longer duration singing bouts with other males, (2) displayed patterns of courting and copulating within the breeding season more typical of wild local cowbirds, and (3) developed song more slowly and of lower potency.
Cowbird song serves two functions in social interactions. It is sung to
females as part of courtship, and it is sung to males to establish intrasexual
social relationships within the flock
(Dufty, 1986). Thus, to breed
successfully, males must develop song effective at eliciting copulatory
postures from females and, just as important, must sing the song. Similar to
females, males can distinguish a high-potency from low-potency song
(West and King, 1986). Singing
a high-potency song can result in aggression from other males. Thus, song
develops as a compromise between intersexual and intrasexual pressures. In the
present study, without adult male influence, the J males assorted less with
other males, interacted less with song with other males, and sang more
undirected song. This relative lack of male social interactions cascaded into
lack of aggressive interactions and lack of competition. In comparison,
juvenile males in the JA condition were more frequently interrupted in
attempts at soliloquies by the arrival or nearby presence of other males.
These juveniles engaged in more male singing interactions and produced less
undirected song. These differences served to launch juveniles in the two
conditions down very different vocal and social developmental trajectories,
influencing song potency and even mating behavior.
Possibly, the observed difference in song potency between JA and J juvenile
males was an artifact of JA males being in a confined area with adults. On
this hypothesis, JA juveniles sang less mature song while in the adults'
presence to allow them to escape negative consequences of aggression by adults
(see Casey and Baker, 1993;
Payne, 1981;
West and King, 1980).
Throughout the extensive observations we made across the study, however, we
found no evidence that adult males conspicuously or continuously dominated or
threatened young males that directed songs to them (although it may not take
extensive feedback for aggression to have an effect). Contrary to an
aggression hypothesis, J juveniles' song was more developed as early as the
fall and winter; times at which adult males in the JA condition rarely
interacted at all with the juveniles.
We suggest that the different learning environments that emerged in the two conditions provided juveniles with different types of reinforcement for their actions, thus influencing their behavioral and vocal development. Adult males behaved and interacted in different ways from juveniles, and when juvenile males interacted with adults, different patterns of singing and social associations by adults provided JA juveniles with different response contingencies to their actions. For example, song practice appears to be related to song potency and song stereotypy, and opportunities for song practice may depend on the contingencies present in the social group.
Additionally, responses to song differed in the two conditions. Adult males
in the JA aviary often responded to song by not moving away from song
overtures. In past work, we have shown that when singing to females, young
male cowbirds appear to be able to modulate song content in a facultative
manner; specifically, young males appear to be sensitive to how often females
stay and how often they respond when males direct a song to them, and males
modify vocal content in response to such behavior
(Smith et al.,
2000,Smith et al.,
2000; West and King,
1988). In the present case, it is possible that a similar
facultative ability when singing to males may have led to opposing effects on
song development.
It is possible that the effects revealed in this study could be
epiphenomena of the unnatural aviary setting or that some other unmeasured
variable in the aviaries could be responsible for the observed findings. Past
work, however, has replicated some of the main effects observed here. For
example, patterns of near-neighbor associations, singing interactions, and
courtship behavior of the birds in the JA condition were similar to the
findings of Smith et al.
(2002), where birds were
housed in the same social composition in an aviary complex four times the size
of the ones used in the current study. Also, the patterns of behavior from the
JA condition are representative of observations made in the field
(King and West, 1988). And
past work replicates the finding that juvenile males with no adult male
feedback do not learn rudiments of counter-singing and display, important
components of intrasexual singing interactions
(Freeberg et al., 1995; West
et al., 1996,
1997). We have also recently
replicated the early effects of adults on juvenile social assortment and
singing patterns in groups of young juveniles that were within weeks of
independence from their hosts (White et
al., 2002,White et al.,
2002). Even in these young birds, the effects of adding or
removing adults from their social group on their behavior were similar to the
effects shown in the present study. For example, juveniles who were housed
without adults had fewer near-neighbor associations and began singing earlier
and more frequently than juveniles housed with adults.
Finally, because we used naturally occurring variation in social groups,
some of the patterns of behavior seen here can be tested in free-living groups
in nature (see Freeberg et al.,
2001, for a comparative study of song structure between two
cowbird populations that also differ in social ecology). The effects seen in
captivity in this study can be used to make testable predictions about spacing
behavior, song potency, and patterns of mating behavior for groups of cowbirds
in the wild, and such a social approach to looking at behavioral development
may be able to explain some of the observed variation in demographics and
behavior reported in the field (Rothstein
and Robinson, 1998). Also, investigations of how variation in
social experience affects development in other species can begin to shed light
on general rules of social organization (see, e.g.,
Adkins-Regan and Krakauer,
2000; Korpela and Sandnabba,
1994; Moore et al.,
1995; Price et al.,
1994).
Developmental ecology
Regardless of the causes of the differences across conditions, the outcome
was clear: developmental reaction norms
(Schlichting and Pigliucci,
1998) for juvenile male social behavior were large and variable.
Such variability is especially striking for a species classically considered
as having a closed developmental system
(Lehrman, 1974;
Mayr, 1974). A benefit of such
a facultative system of development that allows for patterns of behavior to be
organized in response to recurring patterns of social stimulation could be to
permit young cowbirds to enter and conform to the variety of social
environments they may encounter. This research program is in its infancy and
will require more study of how individuals of different ages and sex fit
together in a group to make up a social system. The next phase of this study
will be to see how these different patterns of behavior displayed by the two
groups of juveniles persist into adulthood and to examine the stability of
social groups as new generations of juveniles are introduced. Determining the
mechanisms of cross-generational transmission of information important in
developing typical breeding season behavior, as well as determining the
duration and stability of these behavior patterns, will provide insight into
how selection acts on social behavior over ontogeny.
This paradigm, studying how social factors present in a large social group
can influence development, provides a new means for understanding and
predicting mating behavior. Ecological conditions have traditionally been
considered critical in the evolution of mating behavior
(Emlen and Oring, 1977).
Additionally, ecological conditions experienced throughout development can
influence phenotypic expression. Here, integrating social ecology with an
ontogenetic perspective revealed facultative properties of mating and vocal
behavior that potentially have important evolutionary consequences. These
properties can only be understood by taking into account the social ecology
the birds experienced across development.
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ACKNOWLEDGEMENTS |
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We acknowledge funding from National Science Foundation. D.J.W. received support from a Natural Sciences and Engineering Research Council of Canada postdoctoral fellowship. Sue Linville and Amy Monaco assisted with data collection. Ron Ydenberg, Anne Smith, and two anonymous reviewers provided valuable comments on an early draft of this manuscript. All work was done under ABS guidelines for ethical treatment of animals (Indiana Animal Care and Use Study number 99-108).
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Adkins-Regan E, Krakauer A, 2000. Removal of adult males from the rearing environment increases preference for same-sex partners in the zebra finch. Anim Behav 60: 47-53.[Web of Science][Medline]
Barnard P, 1998. Variability in the mating systems of parasitic birds. In: Parasitic birds and their hosts (Rothstein SI, Robinson SF, eds). New York: Oxford University Press; 339-356.
Beecher MD, 1996. Birdsong learning in the laboratory and field. In: Ecology and evolution of acoustic communication in birds (Kroodsma DE, Miller EH, eds). Ithaca, New York: Cornell University Press; 62-74.
Beecher MD, Campbell SE, Stoddard PK, 1994.
Correlation of song learning and territory establishment strategies in the
song sparrow. Proc Natl Acad Sci USA 91:
1450-1454.
Bell DA, Trail PW, Baptista LF, 1998. Song learning and vocal tradition in Nuttall's white-crowned sparrows. Anim Behav 55: 939-956.[Web of Science][Medline]
Casey RM, Baker MC, 1993. Aggression and song development in white-crowned sparrows. Condor 95: 723-728.
Cristol DA, Baker MB, Carbone C, 1999. Differential migration revisited. Latitudinal segregation by age and sex class. Curr Ornithol 15: 33-88.
Doligez B, Danchin E, Clobert J, Gustafsson L, 1999. The use of conspecific reproductive success for breeding habitat selection in a non-colonial, hole-nesting species, the collared flycatcher. J Anim Ecol 68: 1193-1207.
Dolman CS, Templeton J, Lefebvre L, 1996. Mode of foraging competition is related to tutor preference in Zenaida aurita. J Comp Psychol 110: 45-54.[Web of Science][Medline]
Dufty AM Jr, 1986. Singing and the establishment and maintenance of dominance hierarchies in captive brown-headed cowbirds. Behav Ecol Sociobiol 19: 49-55.
Emlen ST, Oring LW, 1977. Ecology, sexual selection,
and the evolution of mating systems. Science
197: 215-223.
Freeberg TM, 1998. The cultural transmission of courtship patterns in cowbirds. Anim Behav 56: 1063-1073.[Web of Science][Medline]
Freeberg TM, King AP, West MJ, 1995. Social malleability in cowbirds (Molothrus ater artemisiae): Species and mate recognition in the first 2 years of life. J Comp Psychol 109: 357-367.
Freeberg TM, King AP, West MJ, 2001. Cultural transmission of vocal traditions in cowbirds (Molothrus ater) influences courtship patterns and mate preferences. J Comp Psychol 115: 201-211.[Web of Science][Medline]
Friedmann H, 1929. The cowbirds. Springfield, Illinois: CC Thomas.
Galef BG Jr, 1996. Social enhancement of food preferences in Norway rats: a brief review. In: Social learning: the roots of culture (Heyes CM, Galef BG Jr, eds). San Diego, California: Academic Press; 49-60.
Heyes CM, Galef BG Jr (eds), 1996. Social learning in animals: the roots of culture. San Diego, California: Academic Press.
Johnsgard PA, 1997. The avian brood parasites: deception at the nest. New York: Oxford University Press.
King AP, West MJ, 1977. Species identification in the
North American cowbird: Appropriate responses to abnormal song.
Science 195:
1002-1004.
King AP, West MJ, 1988. Searching for the functional origins of cowbird song in eastern brown-headed cowbirds (Molothrus ater ater). Anim Behav 36: 1575-1588.
King AP, West MJ, 1989. Presence of female cowbirds (Molothrus ater) affects focal imitation and improvisation in males. J Comp Psychol 103: 39-44.
Korpela SR, Sandnabba NK, 1994. Gender-specific social experiences and the development of aggressive and sexual behavior in male mice. Aggressive Behav 20: 123-134.
Kroodsma DE, Liu W-C, Goodwin E, Bedell PA, 2000. The ecology of song improvisation as illustrated by North American sedge wrens. Auk 116: 373-386.
Lehrman DS, 1974. Can psychiatrists use ethology? In: Ethology and psychiatry (White NF, ed). Toronto: University of Toronto Press; 187-196.
Mayr E, 1974. Behavioral programs and evolutionary strategies. Am Sci 62: 650-659.[Web of Science][Medline]
Moore AJ, Reagan NL, Haynes KF, 1995. Conditional signaling strategies—effects of ontogeny, social experience and social status on the pheromonal signal of male cockroaches. Anim Behav 50: 191-202.
Morrison ML, Hall LS, Robinson SK, Rothstein SI, Hahn DC, Rich TD (eds), 1999. Research and management of the brown-headed cowbird in western landscapes. Stud Avian Biol 18.
Mottley K, Giraldeau LA, 2000. Experimental evidence that group foragers can converge on predicted producer-scrounger equilibria. Anim Behav 60: 341-350.[Web of Science][Medline]
Mousseau TA, Fox CW (eds), 1998. Maternal effects as adaptations. New York: Oxford University Press.
Nordby JC, Campbell SE, Beecher MD, 1999. Ecological
correlates of song learning in song sparrows. Behav Ecol
10: 287-297.
Nordby JC, Campbell SE, Burt JM, Beecher MD, 2000. Social influences during song development in the song sparrow: A laboratory experiment simulating field conditions. Anim Behav 59: 1187-1197.[Web of Science][Medline]
O'Loghlen AL, Rothstein SI, 1993. An extreme example of delayed vocal development: song learning in a population of wild brown-headed cowbirds. Anim Behav 46: 293-304.
Ortega CP, 1998. Cowbirds and other brood parasites. Tucson: University of Arizona Press.
Payne RB, 1981. Song learning and social interaction in indigo buntings. Anim Behav 29: 688-697.
Payne RB, Payne LL, 1993. Song copying and cultural transmission in indigo buntings. Anim Behav 46: 1045-1065.
Petrinovich L, 1988. Individual stability, local variability and the cultural transmission of song in white-crowned sparrows (Zonotrichia leucophrys nuttalli). Behaviour 107: 208-240.
Price EO, Borgwardt R, Blackshaw JK, Blackshaw A, Dally MR, Erhard H, 1994. Effect of early experience on the sexual performance of yearling rams. Appl Anim Behav Sci 42: 41-48.
Reader SM, Laland KN, 2000. Diffusion of foraging innovations in the guppy. Anim Behav 60: 175-180.[Web of Science][Medline]
Rothstein SI, Robinson SK (eds), 1998. Parasitic birds and their hosts. New York: Oxford University Press.
Rothstein SI, Verner J, Stevens E, 1980. Range expansion and diurnal changes in dispersion of the brown-headed cowbird in the Sierra Nevada. Auk 97: 253-267.
Rothstein SI, Yokel DA, Fleischer RC, 1986. Social dominance, mating, and spacing systems, female fecundity and vocal dialects in captive and free-ranging brown- headed cowbirds. Curr Ornithol 3: 127-185.
Rothstein SI, Yokel DA, Fleischer RC, 1988. The agonistic and sexual functions of vocalizations of male brown-headed cowbirds (Molothrus ater). Anim Behav 36: 73-86.
Schlichting CD, Pigliucci M, 1998. Phenotypic evolution: A reaction norm perspective. Sunderland, Massachusetts: Sinauer Associates.
Smith JNM, Cook TL, Rothstein SI, Robinson SK, Sealy SG (eds), 2000. Ecology and management of cowbirds and their hosts. Austin: University of Texas Press.
Smith VA, King AP, West MJ, 2000. A role of her own: female cowbirds, Molothrus ater, influence the development and outcome of song learning. Anim Behav 60: 599-609.[Web of Science][Medline]
Smith VA, King AP, West MJ, 2002. The context of social learning: association patterns in a captive flock of brown-headed cowbirds. Anim Behav 63: 23-35.
Stamps JA, Krishnan VV, 1999. A learning-based model of territory establishment. Q Rev Biol 74: 291-318.
ten Cate C, Bateson P, 1988. Sexual selection: the evolution of conspicuous characteristics in birds by means of imprinting. Evolution 42: 1355-1358.
West MJ, King AP, 1980. Enriching cowbird song by social deprivation. J Comp Physiol Psychol 94: 263-270.
West MJ, King AP, 1986. Song repertoire development in male cowbirds (Molothrus ater): its relation to female assessment of song. J Comp Psychol 100: 296-303.[Web of Science][Medline]
West MJ, King AP, 1988. Female visual displays affect the development of male song in the cowbird. Nature 334: 244-246.[Medline]
West MJ, King AP, Freeberg TM, 1996. Social malleability in cowbirds: new measures reveal new evidence of plasticity in eastern subspecies (Molothrus ater ater). J Comp Psychol 110: 15-26.[Web of Science][Medline]
West MJ, King AP, Freeberg TM, 1997. Building a social agenda for birdsong. In: Social influences on vocal development (Snowdon CT, Hausberger M, eds). Cambridge: Cambridge University Press; 41-56.
West MJ, King AP, White DJ, in press. Discovering culture in birds: the role of learning and development. In: Social complexity in animals (de Waal FBM, ed). Boston: Harvard University Press.
West-Eberhard MJ, 1983. Sexual selection, social competition and speciation. Q Rev Biol 58: 155-183.
White DJ, King AP, Cole A, West MJ, 2002. Opening the social gateway: early vocal and social sensitivities in brown-headed cowbirds (Molothrus ater). Ethology 109: 23-37.
White DJ, King AP, Duncan SD, 2002. Voice recognition technology as a tool for behavioral research. Behav Res Methods Instrum Comput 34: 1-5.[Web of Science][Medline]
Woolfenden BE, Gibbs HL, Sealy SG, 2001. Demography of brown-headed cowbirds at Delta marsh, Manitoba. Auk 118: 156-166.
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