Ecological effects on song learning: delayed development is widespread in wild populations of brown-headed cowbirds

ANIMAL BEHAVIOUR, 2002, 63, 475–486 doi:10.1006/anbe.2001.1951, available online at http://www.idealibrary.com on

Ecological effects on song learning: delayed development is widespread in wild populations of brown-headed cowbirds ADRIAN L. O’LOGHLEN* & STEPHEN I. ROTHSTEIN†

*Department of Psychology, University of Washington †Department of Ecology, Evolution & Marine Biology, University of California, Santa Barbara (Received 10 January 2001; initial acceptance 8 May 2001; final acceptance 4 September 2001; MS. number: A8964R)

The timing and extent of early exposure to conspecific song can have critical influence on subsequent male vocal development in songbirds. Opportunities to memorize local song models may vary among populations depending on local ecological conditions that determine the length of the breeding season. In populations with comparatively short breeding seasons, such as northern or high-elevation populations, restricted access to local songs may delay development in a large proportion of juveniles. Previous studies have described extreme examples of delayed development in high-elevation populations of brown-headed cowbirds, Molothrus ater, in the Sierra Nevada of California, U.S.A. In the current study, we determined that delayed development also occurs in a low-elevation population located at a more northerly latitude than those in the Sierra. We recorded two kinds of songs from yearling and adult males who had been given testosterone (testosterone increased song output but did not change the nature of songs in males’ repertoires) soon after being trapped at two adjacent sites in New York state, U.S.A. The average size of ‘perched’ song repertoires of 17 yearlings was significantly smaller than that of 20 local adults (2.8 versus 4.6 types, respectively) and yearlings generally lacked the shared songs typically found in adult repertoires. Only 40% of yearlings trapped at one site produced the correct local dialect ‘flight whistle’ compared with 91.7% of adults. These results strongly suggest that juvenile access to local songs is also restricted in this population and that delayed vocal development is widespread in cowbirds. In addition, these findings indicate that reliance on field recordings may underestimate adult–yearling differences in vocal competency in cowbirds because yearlings that sing readily in nature may not be representative of yearlings in general, a result that may also apply to other songbird species. 

O’Loghlen & Rothstein 1993). One such environmental factor is the extent of exposure to conspecific song during the first 3 months of life. Both the timing and duration of this early exposure can be crucial to the ontogeny of learned song. But opportunities for song acquisition by young birds may vary depending on local ecological conditions that determine the length of the breeding season. Due to shortened breeding seasons, hatching-year young in northern or high-elevation populations are likely to experience less exposure to their species’ songs than conspecific young in other populations (Nelson et al. 1995, 1996a; O’Loghlen 1995). Even within the same population, early and late hatching young may experience different levels of exposure to conspecific song during their hatching year and some of the latter may not hear any conspecific song at all (Kroodsma 1996). These types of differences in access to conspecific song in early life may result in inadequate opportunities for song memorization and delayed development in some individuals so that unlike many of their age cohort, these

Most temperate region songbirds are assumed to memorize their species typical songs sometime during the first few months of life and to produce fully developed ‘adultlike’ song by the time they are just under one year old and beginning their first breeding season (Slater 1983; Catchpole & Slater 1995). Many of the key features in this developmental process of song production in male oscines, especially as relates to the timing of certain events, were identified by the classic laboratory studies of Marler and his coworkers (Marler 1970; Marler & Peters 1977). Subsequent investigations have shown that social interactions and other environmental factors that young males are likely to experience in nature can have critical influences (Kroodsma 1978; Kroodsma & Pickert 1980; Payne 1981; Baptista & Petrinovich 1984; Nelson 1992; Correspondence: A. L. O’Loghlen, Department of Psychology, Box 351525, University of Washington, Seattle, WA 98195, U.S.A. (email: [email protected]). Dr S. I. Rothstein is at the Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106, U.S.A. 0003–3472/02/030475+12 $35.00/0

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individuals do not have adult-like song repertories by the start of their first breeding season (Kroodsma 1988; Thielckle & Krome 1989; O’Loghlen 1995). Brown-headed cowbirds, Molothrus ater, offer an exceptional opportunity for studies of the developmental consequences of natural variation in the acquisition phase of song development. Although this species is an obligate brood parasite, the major characteristics of vocal development in cowbirds correspond to those of nonparasitic oscine species and the cowbird is one of the most prominent North American species cited in the bird song literature (e.g. King & West 1977; West & King 1988). Nevertheless, there are features specific to cowbird biology that could result in unusually extensive variation in the amount of early exposure to conspecific song experienced by young cowbirds within and among populations. Because they are reared by host species, cowbirds have limited, if any, experience with adult conspecifics during their first 6–8 weeks of life (for possible exception see Hahn & Fleischer 1995), a crucial time for vocal development in many species. In addition, because breeding activity in cowbirds, including singing, ceases abruptly as soon as hosts and female cowbirds stop laying (Scott 1963; Rothstein et al. 1980), the period during which young cowbirds have the opportunity to hear conspecific song is curtailed compared with many songbirds, most of which continue to sing after egg laying ceases. Thus local ecological factors that affect the breeding phenology of hosts may have a profound effect on the amount of exposure to conspecific song in young cowbirds. Given that at least 144 species are known to have reared cowbirds (Friedmann & Kiff 1985) and that cowbirds occupy a wider range of habitats and are more ubiquitous than any other North American bird (Rothstein 1994), variation in song exposure during the hatching year is likely to be pronounced in this species. In previous studies, we showed that sexually mature yearling (i.e. second-year, SY, in banding terminology) male cowbirds in their first breeding season in the Sierra Nevada of California, U.S.A. display a remarkable degree of delayed vocal development. Their overall vocal repertoires are smaller than those of adult males (at least 2 years old, or after-second-year, ASY, in banding terminology) and the types of songs they produce differ from those of adults in generally being unique to each yearling or shared by only a small proportion of the population (O’Loghlen & Rothstein 1993; O’Loghlen 1995). These Sierran populations (M. a. artemisiae) occur at high elevations (ca. 1850–2750 m) near the altitudinal limit of this species (Rothstein et al. 1980; Verner & Ritter 1983) and therefore have especially short breeding seasons. This raises two important questions. Does such extremely delayed vocal development occur in more typical populations breeding at low elevations if they too have abbreviated breeding seasons? Do populations that experience much longer breeding seasons than in the Sierra, such as southerly ones at low elevations, show more advanced vocal development in yearlings? In this paper, we address primarily the first question by presenting data on vocal development in a low-elevation

cowbird population from upstate New York, U.S.A. A previous study reported that yearlings in this population had generally smaller song repertoires than adults (A. M. Dufty, personal communication), but the difference was not significant statistically (Dufty 1985). However, because this population is far to the north of our Sierran study sites it also has short breeding seasons (Dufty & Wingfield 1986a) and may also have delayed development in other aspects of vocal ontogeny. Furthermore, we chose this New York locality because we wanted to broaden the geographical scope of our vocal ontogeny studies, and because research on captive cowbirds from diverse regions has suggested geographical variation in vocal development (King & West 1990). If vocal development in the New York population is delayed in a manner similar to that in the Sierra, this would strongly suggest that protracted vocal development is widespread in cowbirds and not limited to populations breeding at one extreme (high elevations) of the ecological continuum occupied by this wide-ranging species. Vocal ontogeny in cowbirds is particularly interesting because males have two categories of courtship songs, perched songs and flight whistles (Rothstein et al. 1988; West et al. 1998). In aviary populations, both flight whistle (FW) and perched song (PS) singing behaviour correlate strongly with mating success (West et al. 1981, 1998) and male dominance (West et al. 1981, 1998; Rothstein et al. 1986). Furthermore, both of these vocalizations are associated with copulations in the wild in all three subspecies (Dufty & McChrystal 1992; GorneyLabinger 1997) and both are potent releasers of copulatory postures when played to captive females under controlled conditions (King & West 1977; O’Loghlen & Rothstein 1995, unpublished data). Adult male cowbirds generally have repertoires of two to eight PS types and one FW type (Rothstein et al. 2000), all of which are learned from males resident in a local area (O’Loghlen 1995). Perched songs are used primarily for intra- and intersexual interactions when individuals are separated by short distances (<1 m), while FWs are used most often for interactions involving females and other males at longer distances when individuals are generally out of visual contact (King et al. 1981; Rothstein et al. 1988). Exceptions to these contexts occur immediately prior to and during copulations when both of these vocalizations are produced (Dufty & McChrystal 1992; West et al. 1998), and when solitary males broadcast PSs and FWs (Friedmann 1929; Rothstein et al. 1988). In the Sierra, delayed vocal development may have important reproductive consequences. Even though they are sexually mature, yearling males in these populations have much lower success in obtaining copulations than adults (Rothstein et al. 1986; Yokel & Rothstein 1991). Furthermore, under experimental conditions, females from these populations are more likely to solicit for copulations when played a local FW type than when presented with the foreign or incomplete types typical of yearlings (O’Loghlen & Rothstein 1995, unpublished data). Thus, in the Sierra there is a clear correlation between the limited mating success yearlings experience and the deficit they show in producing local songs. This

O’LOGHLEN & ROTHSTEIN: DELAYED VOCAL DEVELOPMENT

METHODS We trapped male brown-headed cowbirds at the Rockefeller University Field Research Center (RUFRC), Millbrook, New York from 27 April to 25 May 1999, using a large decoy trap (222.6 m) and millet-baited Potter traps. Males were also trapped from 2 to 9 June 1999 at a site (Verbank) 1.7 km northeast of the RUFRC using Potter traps. Each bird was uniquely colour banded, subjected to a standardized set of morphological measurements (as in Fleischer & Rothstein 1988) and aged as a yearling or adult based on retention of juvenile underwing coverts, as described by Selander & Giller (1960). The latter authors estimated that about 5% of yearling males replace all of their juvenile underwing coverts and therefore would be incorrectly aged as adults. Ortega et al. (1996) suggested that the error rate is higher, as they reported that four of 11 males known to be yearlings on the basis of prior banding had no juvenile coverts, although they report that all birds aged as yearlings were in fact yearlings. They also reported that all birds known to be adults on the basis of banding were correctly aged as adults via plumage. Thus there are three categories of males, yearlings that retain juvenile coverts, yearlings with adult coloured coverts and true adults. Given that Selander & Giller’s ageing criteria cannot distinguish between the two latter categories, a small proportion of the males we classified as adults may have been yearlings. The impact this may have on our study is likely to be small for two reasons. First, because some birds we aged as adults may have been yearlings, our adult–yearling comparisons are conservative (i.e. we might have found even stronger vocal differences if all yearlings had been correctly identified). Second, Ortega et al. state explicitly that they did not assess the greater primary and greater secondary coverts while looking for juvenile feathers. By contrast, Selander & Giller assessed these two feather types and reported that yearlings were especially likely to retain juvenile feathers in these tracts. We also assessed these two tracts and therefore our error rate in ageing yearlings was likely to have been the same as the near negligible 5% rate that Selander & Giller reported. The birds were held at the RUFRC in individual cages (603652 cm), visually but not acoustically isolated from each other, for 1–8 days after capture until a cohort of six individuals was available. As reported in a previous study using similar housing arrangements, there was no evidence that auditory contact had any inhibitory effect on the willingness of the yearlings to vocalize, nor on the songs they produced (O’Loghlen & Rothstein 1993). Handling and feeding (wild bird seed ad libitum) was identical for all birds and they were maintained under the natural photoperiod for the area.

(a)

(b)

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apparent link between mating success and vocal development was yet another reason for our decision to study vocal development in the New York population. Yearling males from this region have been reported to have the same mating success as adults (Dufty 1982), suggesting that they may be as vocally proficient as adults.

Yearling 21

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Figure 1. Audiospectrograms of two perched song (PS) types each recorded from a different yearling before (a) and after (b) they were given testosterone. There were no systematic differences observable in the structure of PSs recorded under these two circumstances. All of the PSs shown in this and later figures were recorded in isolation chambers and neither the song recordings nor the spectrograms were processed in any way.

We gave all cohort males (except one, see below) testosterone implants to encourage vocal ouput and to overcome their reluctance to give FWs in captivity (O’Loghlen & Rothstein 1993). We inserted a Silastic implant (1.69 mm outer diameter; Dow Corning, Midland, Michigan, U.S.A.) packed with testosterone (10 mm; Sigma Chemical Co., St Louis, Missouri, U.S.A.) through a small incision (2–3 mm) in the skin on the left side of the chest of each bird. We sealed the incision with Nexaband glue (Closure Medical Corp., Raleigh, North Carolina, U.S.A.). This procedure is quick (<3 min), minimally invasive and the birds resumed normal behaviour soon after their return to their individual cages, as has been reported in other studies using similar procedures (e.g. Hunt et al. 1997). An increased frequency of singing due to steroid treatment is normally observed after 2–3 days (Balthazart 1983) and this was confirmed in our study birds. Naturally occurring testosterone blood levels in our study population peak in mid-April (Dufty & Wingfield 1986b), preceding the date when the first birds were implanted (30 April) for the current investigation. Yearling males in this population have fully developed testes and naturally elevated testosterone levels comparable to those of adults and, unlike other songbirds, testosterone remains closer to peak levels in cowbirds for most of the breeding season (Dufty & Wingfield 1986b). Given that elevated levels of testosterone are associated with song crystallization in songbirds (see references in Brenowitz 1997), it is parsimonious to assume that the songs of both yearlings and adults were fully crystallized prior to the administration of implants. In support of this, PSs recorded from a subset of males (N=6), two of which were yearlings, prior to and after the administration of testosterone were identical, confirming that testosterone changes the quantity but not the nature of the songs a male sings (see examples in Fig. 1). Furthermore, and as found in previous studies using the same procedures, there was no evidence in the present

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study that yearlings trapped later in the season were more advanced in their development of local repertoires than yearlings trapped earlier (O’Loghlen & Rothstein 1993; O’Loghlen 1995). If vocal development in yearlings continued to proceed during the course of the season, then birds trapped later in the season would have had more adult-like repertoires. This lack of difference between yearlings trapped early and late in the season supports the proposal that vocal development is frozen at the start of the breeding season, probably because of the loss of developmental plasticity (i.e. song crystallization) associated with naturally elevated levels of testosterone (Brenowitz 1997). On the morning of the fourth day after receiving their implant, we transferred each bird in turn to a smaller cage (462326 cm), which was then placed in a fabriclined attenuation chamber (542830 cm) fitted with a Realistic 3 (7.62 cm) speaker. After 3 min of acclimatization in the chamber, we played a standard recording of female chatter (Friedmann 1929; Burnell & Rothstein 1994) from a Sony Professional Walkman cassette recorder to the test male and recorded his responses using a Realistic ‘tie-pin’ condenser microphone and an Optimus SCT-86 stereo-cassette recorder. We then placed a mirror in the chamber to encourage males to produce PSs. The combination of a mirror and playback of lowvolume chatter stimulated most males to produce a rapid series of PSs. Males were recorded for 30 min in the chamber and the majority produced our target of a minimum of 30 PSs within that period. Cowbirds tend to run through their PS repertoire quickly, and for eastern cowbirds, a recording session of 12 or more songs is likely to contain a male’s full PS repertoire (West et al. 1983; Dufty 1985). The following morning, day 5 after implantation, we individually placed males ‘out of doors’ in their cages and recorded their vocalizations using a Sennheiser MKH 816T microphone and Sony Professional Walkman cassette recorder as they interacted vocally with the local wild cowbirds. We also recorded responses to playback of local and foreign FWs and other cowbird vocalizations. If we did not obtain sufficient recordings from a bird under these procedures, we placed the bird’s cage beside another male’s cage and recorded any vocal interactions. Later that day we removed the birds’ implants and released them at their respective capture sites. As reported previously (O’Loghlen & Rothstein 1993), there were no differences in the PS and FW types produced by males in the different recording contexts. One yearling male recorded without testosterone was slightly injured during the implant procedure and was released after we determined that the injury would not impede its normal behaviour. We did not have an opportunity to elicit FWs from this male. However, PSs recorded from this male and from other males prior to the administration of testosterone were included in analyses. We digitally sampled recordings at 26 kHz using Syrinx software running on a Quantex Pentium II Pro 266 mHz laptop computer. We saved audiospectrograms of all FWs given by each male as wave files on the computer and printed representative examples of every different FW

type and any variants on a Xerox DocuPrint P8 printer. One of us (A.O’L.) viewed all of the PSs recorded from each male as audiospectrograms on the computer and categorized them as different types based on all structural elements visible, including the low-frequency note clusters at the start of the songs, middle elements and the ‘whistles’ at the end (King et al. 1980). Perched songs in an individual cowbird’s repertoire are structurally distinct and cowbirds show high stereotypy in their renditions of PS types. Independent assessment of PS categorization is redundant as numerous studies have demonstrated extremely high concordance (>90%) among independent judges that categorize PSs as different types (Dufty 1985; West & King 1986; O’Loghlen & Rothstein 1993). We saved a representative example of each different PS type and any variants of types as wave files on the computer. Using these saved files we prepared and printed Syrinx spectrographic displays of PS repertoires for each male. We categorized PSs in individuals’ repertoires as ‘shared’ types (present in the repertoire of at least one other male of either age class), or ‘unique’ (not present in any other repertoire) as in a previous study (O’Loghlen & Rothstein 1993). Determining whether a PS is shared is straightforward because cowbirds show high fidelity in copying songs (Dufty 1985). We also prepared a catalogue of all of the different PS types recorded from adult males and used it to categorize PSs as local adult-shared types. As in a previous study, we defined local adult-shared songs as types found in the PS repertoires of two or more locally trapped adults (O’Loghlen 1995). We each categorized PSs as unshared or local adult-shared and there was greater than 90% agreement on these categorizations. We compared results for the Millbrook, New York area with those from previous equivalent vocal studies conducted in FW dialects in the Eastern Sierra Nevada of California. These dialects are located in a region centred around the town of Mammoth Lakes and detailed descriptions of these dialects can be found in Rothstein & Fleischer (1987) and O’Loghlen (1995).

Data Analyses We used Fisher’s exact tests to compare numbers of males producing different categories of song and Mann– Whitney U tests to compare numbers of songs produced by each age class, and for pairwise comparisons of PS repertoire sizes among dialect areas. We used Spearman rank correlations to evaluate associations between variables. We performed all nonparametric statistical tests using Statistica (StatSoft, Inc. Tulsa, Okalahoma, U.S.A.) and all probabilities are two-tailed. RESULTS We trapped 25 males at the RUFRC site and 12 at Verbank. We aged 13 (52%) of the males from RUFRC and seven (58%) from Verbank as adults. We recorded flight whistles from 33 of the 36 males (91.7%) tested. The one yearling male that was released prior to undergoing the full test procedures (see above) was excluded from the FW

O’LOGHLEN & ROTHSTEIN: DELAYED VOCAL DEVELOPMENT

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Figure 2. Audiospectrograms of the three Rockefeller FW variants produced by 11 adults trapped at the Rockefeller site. Not all adults produced all three variants (see text for details). The three distinct structural elements involved in producing these FW variants are indicated by numbers.

data set. Nineteen of 20 adults (95%) and 14 of 16 yearlings (87.5%) produced at least one FW and there were no differences between sites or age classes in the proportion of individuals that produced FWs. An average of 12.6 FWs were recorded per male, and although the average for adults (15.4 FWs) was greater than that for yearlings (9.0), this difference was not significant. All 37 males produced a sufficient number of PSs to estimate full repertoire sizes with an average of 46.5 (3.1 SE) songs per male (range 16–91). There were no significant differences in the numbers of PSs recorded from adults and yearlings, means being 50.8 and 41.5, respectively.

Characterization of the Rockefeller Flight Whistle Dialect Twelve of 13 adults trapped at the RUFRC site produced FWs and 11 of these males (91.7%) sang at least one of the three variants of FWs shown in Fig. 2. These variants (hereon referred to as Rockefeller FWs) are composed of one or two basic elements (elements 1, 2, 3 in Fig. 2). On occasion, element 1 was produced on its own and therefore also functions as a ‘single syllable’ vocalization (Rothstein et al. 1988). The majority of adults (83.3% of 12) produced variant ‘A’ shown in Fig. 2 and 74.3% of 214 FWs recorded were this variant. This is the most commonly heard FW in nature in the vicinity of RUFRC (unpublished data). Flight whistle variant ‘B’ (4.7% of recorded FWs) was produced by five adults, and ‘C’ (20.6% of FWs), by eight. One male produced ‘C’ exclusively and he accounted for the majority of ‘C’ whistles produced (56.8%; 25 of 44). Three adults produced all three FW variants and there was no correlation between the number of FWs recorded and number of Rockefeller FW variants produced by adults (Spearman rank correlation: rS =
0.74, N=11, P=0.83). The remaining Rockefeller adult that gave FWs, did a nonlocal FW type (Fig. 3, Male 19). This pattern of local dialect variation in

Figure 3. Audiospectrograms of non-Rockefeller FWs produced by one adult (M19) trapped at the Rockefeller University Field Research Center (RUFRC) and four adults (Males 36, 30, 25, 34) trapped at the Verbank site. Males 19 and 36 produced the same type of FW. The FW produced by M25 was also recorded from one yearling trapped at Rockefeller. Each mark shown on the time axis represents 0.5 s.

which FWs can be composed of combinations of a number of different song elements is somewhat atypical. However, the Round Valley and Lee Vining dialects of the Eastern Sierra Nevada also show this type of variation (Rothstein & Fleischer 1987; O’Loghlen 1995). Only three of seven adult males (42.9%) trapped at Verbank produced any of the Rockefeller FW variants. This proportion was significantly different from that for the Rockefeller site (Fisher’s exact test: P=0.04) indicating that Verbank is on the border of, or in a different FW dialect area (Rothstein & Fleischer 1987), a result also indicated by fieldwork in areas surrounding the Rockefeller and Verbank sites (unpublished data). Therefore, we have excluded males trapped at this site from our analyses of FW data. Audiospectrograms of FWs from all four Verbank adults not producing Rockefeller whistles are shown in Fig. 3.

Flight Whistles of Rockefeller Adults and Yearlings Along with the 13 adults, there were 11 yearlings trapped at the Rockefeller site. Ten of these yearlings produced FWs and four of these (40%) gave Rockefeller FWs. However, of the birds that produced FWs, adults were significantly more likely to give at least one of the three Rockefeller FW variants than yearlings (Fisher’s exact test: P<0.01 for 11/12 adults versus 4/10 yearlings). Adults also tended to produce more of these FW variants than yearlings, although this difference was not significant. Average number of local FW variants for adults was 2.2 (0.2 SE) versus 1.0 (0.4) for yearlings. One yearling produced all three Rockefeller FW types, and three gave type ‘A’ exclusively. All of the remaining six yearlings produced non-Rockefeller FW types. There was no significant difference between the average of 17.5 FWs (median 12.0; range 0–50) recorded from adults and that of 10.2 whistles for yearlings (median 10.0; range 0–22) trapped at the Rockefeller site (Mann–Whitney U=49.5, N1 =12, N2 =10, P=0.34).

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12 10 8 6 4 2 0

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Figure 4. Frequency distribution of perched song (PS) repertoire sizes by age class showing that adults had significantly larger repertoires of perched song types than yearling cowbirds (Mann– Whitney U test: U=28.0, N1 =20, N2 =17, P<0.001). The data are based on recordings from 37 males trapped at the Rockefeller and Verbank sites.

Thus yearling cowbirds trapped at the RUFRC differed in their FW behaviour from local adults. Yearlings were less likely to produce any of the variants of the local Rockefeller FW type and those that did tended to have fewer variants than local adults.

Perched Songs of Adults and Yearlings There was no correlation between the number of PSs recorded and repertoire size for adult (rS =
0.06, N=20, P=0.80), or yearling males (rS =
0.11, N=17, P=0.66). Unlike the situation with the local FWs, males trapped at the Rockefeller and Verbank sites did not differ in PS types. In particular there was no difference in the proportions of PS repertoires composed of local adult-shared PS types (see below) for all males from each site and this was also true for adult males from these two sites. We have therefore included males from both sites in our analyses of PSs (hereon we will refer to this combined sample as Millbrook males). This result of greater microgeographical variation in FWs than in PSs is typical of other cowbird populations (S. I. Rothstein, unpublished data). Repertoire sizes for 17 yearlings averaged 2.8 (0.2) PS types, which was significantly smaller than the average of 4.6 (0.2) for 20 adults (Fig. 4; Mann–Whitney U test: U=28.0, N1 =20, N2 =17, P<0.001). Despite their larger repertoires, only five adults (25%) ever produced a unique PS type (one produced by no other bird of either age class), while 13 (76.5%) of the yearlings did so (Fisher’s exact test: P<0.01). Fifteen adults (75%) shared all of their song types with at least one other bird of either age class, while only four of the yearlings (23.5%) had repertoires based solely on shared songs (Fisher’s exact test: P<0.01). As described below, there was only one song type that was shared by two or more yearlings and that was absent from all adult repertoires. Adult repertoires were composed for the most part of a selection from among nine local adult-shared PS types. The repertoires of 15 of the 20 adults (75%) were made up entirely from these songs and the mean percentage of

Average number of PS types

ANIMAL BEHAVIOUR, 63, 3

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Figure 5. Average PS repertoire sizes (±SE) and proportions of adult-shared PS types in repertoires by age class. Adult-shared PSs are types that were found in the repertoires of two or more locally trapped adults. Locally shared PS types made up a significantly larger proportion of the repertoires of adults than yearlings (Mann– Whitney U test: U=25.0, N1 =20, N2 =17, P<0.001). In general, nonlocal PSs are types that are not shared by males in either age class (see Fig. 6). Medians and ranges refer to numbers of adultshared PS types. Sample sizes are shown in parentheses.

local-shared songs in adult repertoires was 89.0%. Of the 10 nonadult-shared types in adults repertoires, seven (70%) were recorded from three males that gave nonRockefeller FWs. In contrast to adults, only three of the 17 yearlings (17.6%) had repertoires composed entirely of local adult-shared songs and the average proportion of adult-shared types in yearling repertoires was 44.7% (Fig. 5; Mann–Whitney U test: U=25.0, N1 =20, N2 =17, P<0.001). Furthermore, while all adults had at least one local PS type in their repertoires, six yearlings had none of these types (Fisher’s exact test: P<0.01 for 0/20 versus 6/17 for males with no local PSs). One PS type was shared exclusively among four yearlings. This PS (Yearling 17, PS ‘A’ in Fig. 6), occurs throughout the range of the three cowbird subspecies, and in some populations it occurs in much higher frequencies in both adult and yearling repertoires than in the current study (Dufty 1985; O’Loghlen & Rothstein 1993; O’Loghlen 1995). In summary, adult cowbirds trapped at the Rockefeller and Verbank sites had significantly larger repertoires of PS types than yearlings. The vast majority of PSs in adult repertoires were types that were shared with other birds and most adults had repertoires composed entirely of types that were shared with other local adults. In contrast, few yearlings had repertories based entirely on shared PSs, and for the most part, yearling repertoires were composed of unique PS types not found in the repertoires of other males of either age class. DISCUSSION Much of our knowledge of song development derives from studies involving male songbirds exposed to controlled learning regimes in captivity. While such studies elucidate the range of learning capabilities within various species, they do not necessarily reveal the developmental processes that occur in nature (Beecher 1996; Kroodsma 1996). Our results from the Millbrook study and those

O’LOGHLEN & ROTHSTEIN: DELAYED VOCAL DEVELOPMENT

Adult 6 10

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0.5 Time (s) Figure 6. Audiospectrograms of perched song (PS) repertoires of adult and yearling male cowbirds. Adult 6 had a repertoires of five PS types, all of which were local adult-shared types (see text and Fig. 5 for explanation). Adult 19 shared all of his four types with Adult 6. Yearlings 35 and 17 had repertoires of three types each. Yearling 35 had one adult-shared type (B) and Yearling 17 none. PS type ‘A’ of Yearling 17 was the only type shared exclusively by yearlings. Each mark shown on the time axis represents 0.5 s.

from the Sierra are remarkably consistent and clearly indicate that delayed development is widespread in cowbirds. These findings are notable because they provide us with insights into the way in which vocal development occurs in nature and how ecological factors can affect song development in the wild. Individuals in avian populations that experience relatively short breeding seasons are likely to have less opportunity, on average, to acquire local songs than individuals in populations with longer seasons. Singing in adult songbirds generally declines as the season progresses (Catchpole & Slater 1995), and in a population with a curtailed season, a larger proportion of nestlings are likely to fledge when singing activity is in decline or has already ceased, than in populations with longer seasons. The extent, if any, to which this difference in opportunity to hear adult song will affect vocal development depends on the species involved and the degree of difference between populations in breeding season duration. Environmental factors that are likely to have the greatest impact on the duration of the avian breeding season include differences in latitude, elevation and climate. Ecological factors likely

to influence the effects of delayed access on development include whether a population is migratory or sedentary, and the number of breeding attempts within a single season, although to a large extent the latter will be contingent on the above environmental factors. Recent evidence for some of these effects have been documented in laboratory studies that compared vocal development in sedentary and migratory populations of whitecrowned sparrows, Zonotrichia leucophrys, and in intrasubspecific comparisons of populations at differing latitudes (Nelson et al. 1996b; Whaling et al. 1998; Nelson 1999). The strongest evidence to date of naturally occurring delayed development comes from studies of migratory montane populations of cowbirds in the eastern Sierra Nevada of California (O’Loghlen & Rothstein 1993; O’Loghlen 1995). The breeding season in these highelevation populations is abbreviated because of the late arrival of spring. Based on the presence of oviducal eggs (i.e. eggs that would be laid within 24 h) in wild-caught females, Fleischer et al. (1987) estimated that breeding in Sierran cowbirds starts in mid- to late May and finishes

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Table 1. Numbers of adult (ASY) and yearling (SY) cowbirds producing different categories of flight whistles (FWs) by dialect area, based on all males producing at least one FW vocalization Complete local FW

Incomplete local FW

Foreign FW

Dialect

ASY (%)

SY (%)

ASY (%)

SY (%)

ASY (%)

SY (%)

Rockefeller, NY Round Valley, CA Convict, CA Mammoth, CA

11 (91.7) 14 (82.3) 16 (88.9) 10 (90.9)

4 (40.0) 1 (5.3) 6 (30.0) 2 (12.5)

0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

0 (0.0) 3 (15.8) 7 (35.0) 10 (62.5)

1 (8.3) 3 (17.6) 2 (11.1) 1 (9.1)

6 (60.0) 15 (78.9) 7 (35.0) 4 (25.0)

NY: New York; CA: California.

in early July. Thus by the time most fledgling cowbirds become independent (after mid-July), cowbird breeding activity has generally ceased and juveniles have limited, if any, opportunity to learn local songs. Consequently, the majority of yearling males in their first season in these populations show pronounced deficits in their production of these local songs. The length of the breeding season for cowbirds at Millbrook is similar to that in the Sierra although it appears to start a week or so earlier (Dufty & Wingfield 1986a). Dufty & Wingfield reported that cowbird breeding activity at Millbrook started in early to mid-May and continued through to late June/early July, based on the presence of large yolky follicles in females. Consistent with these data, independent fledgling cowbirds were reported to first appear in numbers towards the end of June and were abundant in July during the 1991–1993 seasons (C. Hahn, unpublished data). During the present study, the number of adult cowbirds observed and heard at the RUFRC declined noticeably during the first week of July and singing had virtually ceased by the second week (A. L. O’Loghlen, personal observation). Thus many Rockefeller juveniles appear to have limited opportunities to hear local adults sing, as in the Sierra. In the Sierra, however, the breeding season is abbreviated because of the ecological conditions associated with high elevations, whereas in the low-elevation Millbrook area, the season is posited to be curtailed because of its more northerly location. The distribution of cowbirds extends further north than the Millbrook area and it is possible that the effects of restricted access to local songs may be even more pronounced in populations at more northerly latitudes. A recent study of a cowbird population in Manitoba, Canada reports a breeding season from late May to early July, very similar to that in the Sierra (Alderson et al. 1999). However, the vocal behaviour of males in this population has not yet been investigated. Instead of the memorization phase for learning being constrained in juveniles due to short breeding seasons, the widespread delayed learning demonstrated in this study and our prior Sierran work could mean that delayed development is inherent in all cowbird populations. The obvious test of this is a replication of the current study at far southern low-elevation sites with longer breeding seasons. These populations should have more yearlings with adult-like vocal repertoires than found in the Sierra

and New York if our hypothesis that delayed learning is a constraint imposed by short breeding seasons is valid. In accord with this hypothesis, a higher proportion of yearlings in southern California populations (Santa Barbara and Ventura counties) have adult-like repertoires than we found in the Sierra and at Millbrook. For example, 50–60% of Californian yearlings gave complete and correct renditions of the local dialect FW (S. I. Rothstein, unpublished data).

Delayed Development in New York and California Populations Flight whistles In the present study, 91.7% of adult males trapped at the RUFRC produced a local FW type. This compares with a combined average of 87.0% (40 of 46) for adults in the three dialect populations (range 82.3–90.9%) studied in the Sierra Nevada (Table 1). In all dialects, FWs produced by adults were the types most frequently heard from wild males in these respective areas (Rothstein & Fleischer 1987; O’Loghlen 1995; unpublished data), and the proportion of adults with the correct local whistle did not differ among the dialects. Yearlings, on the other hand, rarely produced a complete (see below) and correct local FW. In the Sierran Round Valley dialect only one of 19 yearlings (5.3%) gave the correct and complete local whistle, while Rockefeller had the largest proportion, with 40% of 10 yearlings doing so. Overall, only nine of 55 (16.4%) yearlings in the Sierra had the complete local FW of the dialect area in which they were trapped (O’Loghlen 1995). In the Sierra, a number of yearlings in each of the dialects consistently produced incomplete versions of the local FW type (O’Loghlen 1995). These incomplete FWs were highly stereotyped and were just as likely to be found in yearlings trapped later in the season as those trapped earlier. This phenomenon was most pronounced in the Mammoth dialect where the majority of yearlings (Table 1) produced incomplete versions of the local whistle (O’Loghlen & Rothstein 1993). However, none of the Rockefeller yearlings tested gave an incomplete local whistle. Among the four Rockefeller yearlings that gave local FW types, one produced all three variants (Fig. 2) and the remaining three, just the ‘A’ variant. It is possible that the absence of incomplete local whistles in the

O’LOGHLEN & ROTHSTEIN: DELAYED VOCAL DEVELOPMENT

Table 2. Estimated average perched song (PS) repertoire sizes of adult (ASY) and yearling (SY) cowbirds based on all perched song (PS) types and on types detected in two or more local adult repertoires (adult-shared PS) PS repertoire sizes (±SE)* Area Millbrook, NY Round Valley, CA Convict, CA Mammoth, CA

Local adult-shared PS repertoire sizes (±SE)

N

ASY

SY

ASY

SY

ASY

SY

4.6±0.2 4.0±0.3 4.4±0.4 5.5±1.4

2.8±0.2 3.7±0.2 2.8±0.2 3.1±1.2

4.1±0.3 4.0±0.3 4.4±0.4 4.5±0.2

1.2±0.3 1.5±0.2 1.8±0.2 0.8±0.1

20 9 10 6

17 15 15 13

NY: New York; CA: California. *Repertoire sizes in California dialects are based on males that gave at least eight PSs. Millbrook repertoires are based on males that gave at least 16 PSs.

Rockefeller dialect relates to the comparatively simple structure of the local FW.

Perched song repertoires Adults trapped at the Millbrook sites had PS repertoires with three to seven song types and 4.6 types on average. This is very similar to the results for the three dialect populations studied in the Sierra, where adult repertoires ranged in average size from 4.0 to 5.5 types depending on location and 4.5 types for all three dialects combined (Table 2). With the exception of the Round Valley, California area (see below), adult repertoires were significantly larger than those of yearlings in all dialects (O’Loghlen 1995). In the Sierra, yearlings had repertoires ranging in size from 2.8 to 3.7 types depending on dialect, compared to the 2.8 average for Millbrook. In the Round Valley, yearlings had near adult-sized repertoires (mean 3.7 types) that were significantly larger than the average yearling repertoire in the other dialects (O’Loghlen 1995) including those at Millbrook (Mann– Whitney U test: U=53.5, N1 =15, N2 =17, P<0.01). The Round Valley is at the lowest elevation of the Sierran dialects studied and it is possible that yearlings that disperse into this dialect come from natal populations even lower in elevation where the breeding season is longer and where cowbirds have greater opportunity to memorize more PS types during their hatching year. The majority of adults in all populations we have investigated to date have repertoires largely composed of PS types that are common to other birds in the local dialect population. Most have repertoires consisting entirely of these shared types and few adults produced ‘unique’ or nonshared songs. In the Sierra, 35 of 43 adults (81.4%) had repertoires composed exclusively of types shared with other locally trapped birds, compared with 15 of 20 New York adults (75%) in this study. In contrast, only eight of 54 Sierran yearlings (14.8%) had repertoires of this kind (O’Loghlen 1993), while the equivalent number for Millbrook was four of 17 yearlings (23.5%). Furthermore, the majority of yearlings in all dialects had one or more ‘unique’ songs in their repertories and, in most cases, this category of song accounted for the major part of yearling repertoires (O’Loghlen 1993).

Besides the higher levels of sharing shown by adults relative to all males within each dialect area, we observed even higher sharing exclusively within adult cohorts. So we defined a set of local adult-shared song types based on whether a song was present in the repertoires of two or more adults trapped in a local area (O’Loghlen 1993). The number of such adult-shared songs in the Sierran dialects ranged from seven to nine depending on location and in total, 88.0% of adults (22 of 25) with at least eight PSs recorded (O’Loghlen & Rothstein 1993) had repertoires composed solely of these types (Table 2). There was a total of nine such songs detected at Millbrook and, as in the Sierra, the majority (75%) of local adults had repertoires consisting entirely of these adult-shared song types. There were no differences among the four populations in the extent to which adult repertoires were composed of these local adult-shared songs (Table 2). In contrast, few yearlings in any of the four populations had repertoires composed entirely of local adult-shared PSs. In the Millbrook population, only three of 17 yearlings (17.6%) had repertoires consisting completely of these types and, in the Sierra, this proportion was lower with just four of 43 (9.3%) yearlings having this kind of repertoire. None the less, less than half of the songs in the average Millbrook yearling’s repertoire were local types and equivalent proportions in the Sierra ranged from 64.3 to 27.5% depending on the dialect. Similar to our results, Dufty (1985) reported that there were seven and 11 shared PS types at RUFRC in 1981 and 1982, respectively, and that there were nine shared types in 1979 at a Binghamton, New York site about 290 km to the west. It is likely that adults were responsible for most of the song sharing, as A. M. Dufty (personal communication) found that they had more song sharing than yearlings. Many of the PS types identified by Dufty were produced exclusively by one male, as was the case with our results. We found these ‘unique’ songs to be characteristic of yearling repertoires. Dufty reported that their occurrence tended to be highly transient in the population, and that again is consistent with our observations in the Sierra. In the Sierra, birds recorded as yearlings and again a year later as adults had dropped these ‘unique’ PSs from their

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repertoires during the process of completing their adult repertoires (O’Loghlen 1995).

Spatial Variation in Flight Whistles versus Perched Songs In our analysis of PSs, we included males from two Millbrook area sites that appear to be near or on the borders of two different FW dialects. Although the occurrence of specific PS types is spatially variable (Dufty 1985; O’Loghlen 1995), changes in FWs occur over smaller distances and are more pronounced. Adjacent FW dialects in the Sierra may have PS types common to adults in both areas and also types that are shared by adults exclusively in each dialect. For example in the Mammoth dialect there were eight local adult-shared PS types, three of which were not found in the repertoires of an equivalent sample of adults from the adjacent Convict, California dialect (A. L. O’Loghlen, unpublished data). By contrast, nearly all adults in adjacent Sierran FW dialects give FWs characteristic of their dialect area and different from the ones in adjacent dialects (Rothstein & Fleischer 1987; O’Loghlen 1995). In the present study, adults with non-Rockefeller FWs had smaller local adult-shared PS repertoires than adults with Rockefeller whistles (Mann– Whitney U test: U=13.5, N1 =5, N2 =14, P<0.05). Most of these former males (4 of 5) were trapped at Verbank, the site located on the border of, or possibly in, a different FW dialect area than the Rockefeller site. There was no overlap in the occurrence of PS types at New York sites approximately 290 km apart (Dufty 1985), all of which suggests that PS types change markedly with distance, albeit over distances greater than is the case for FWs.

Field versus Captive Recording and Detection of Delayed Development Dufty (1985) was the first to demonstrate PS sharing in populations of wild cowbirds. Subjects for one of his study populations were trapped and banded at RUFRC during 1981 and 1982, and recorded singing in the wild. However, differences in methodology between his study and ours limit potential comparisons between the two studies. For example, Dufty did not report on FW behaviour. Furthermore, although Dufty’s results were not presented by age class, he stated that there was no difference between yearlings and adults in PS repertoire size. This discrepancy with our results from the same area could be explained if recording male cowbirds singing spontaneously in the wild does not sample the age classes equally. For example, yearlings with small repertoires or inappropriate song types may be reluctant to vocalize in nature for fear of aggression from dominant adults, whereas yearlings with more adult-like repertoires may be more dominant and likely to sing. Thus field recordings of wild males may include disproportionately high numbers of yearlings with large ‘adult-like’ vocal repertoires and few with the smaller, unshared repertoires more typical of most yearlings. Field recordings in the Sierra support this explanation. Nine of 14 (64.3%) Sierran

yearlings from whom FWs were recorded in the field, did the correct FW type for their dialect (Rothstein & Fleischer 1987), whereas only nine of 55 (16.4%) yearlings recorded after being captured and being treated with testosterone (O’Loghlen 1995) did so (Fisher’s exact test: P<0.001). Clearly, we would have underestimated the degree of difference in adult and yearling vocal development in the Sierra had we based our conclusions solely on field recordings.

Conclusion It is evident that a variable but sizable proportion of yearling males in our study populations had not completed their vocal development by their first breeding season. Young cowbirds are obviously capable of developing adult-like vocal repertoires by this age as evident by the occurrence of small numbers of ‘adult-like’ yearlings in all study populations. Longitudinal studies of banded birds in the Sierran populations show that young cowbirds in these dialect areas complete their vocal development sometime between the end of their first and the start of their second breeding season. During this period they learn either to complete their version of the local FW or to switch FW type completely from a foreign to the local type of the area where they spent their first season. When males in the Sierra return from wintering for their second season they have enlarged PS repertoires based on the local PS types of the dialect area where they spent their first season. These changes to their repertoires can be dramatic, with males typically adding multiple local adult-shared types and dropping types that were not locally shared (O’Loghlen & Rothstein 1993; O’Loghlen 1995). Given the yearling–adult differences documented here, it is reasonable to assume that males in New York complete their vocal development in a similar manner. Cowbirds do not have unique processes in their song development that would distinguish them from many other songbirds. Their parasitic lifestyle does provide some special research opportunities because of the natural isolation from conspecifics they experience during the early stages of life. The effects of delayed vocal development documented in our studies may be exaggerated in cowbirds but they are likely to occur in other species also (Kroodsma 1988; Thielckle & Krome 1989; Whaling et al. 1998). However, it is possible that effects of naturally occurring delayed development in other species go undetected because conclusions based on field recordings do not reflect the vocal proficiency of the total yearling cohort. Acknowledgments Our special thanks to Robert Eckard for his invaluable assistance working with us in the field. We also thank Fernando Nottebohm and all of the people at the Rockefeller University Field Research Center at Millbrook, who helped make our time at the Center exceptionally pleasant and productive. We are especially appreciative of the assistance provided to us by Tim Gale and Pat Tellerday. We thank John Burt for providing us with his

O’LOGHLEN & ROTHSTEIN: DELAYED VOCAL DEVELOPMENT

excellent Syrinx software and C. Hahn for access to her unpublished data. Our thanks also to the staff at the Marine Science Institute, UC Santa Barbara for providing administrative support. This project was supported by NSF grant IBN No. 9728091 to S. I. Rothstein and A. L. O’Loghlen. Birds used in this study were trapped, banded and maintained in captivity under the appropriate Federal and State permits, and under IACUC protocols approved by U.C. Santa Barbara (Protocol No. 185) and Rockefeller University. References Alderson, G. W., Gibbs, H. L. & Sealy, S. G. 1999. Determining the reproductive behaviour of individual brown-headed cowbirds using microsatellite DNA markers. Animal Behaviour, 58, 895–905. Balthazart, J. 1983. Hormonal correlates of behavior. In: Avian Biology VII (Ed. by S. Farner, J. R. King & R. A. Parkes), pp. 221–236. New York: Academic Press. Baptista, L. F. & Petrinovich, L. 1984. Social interaction, sensitive phases and the song template hypothesis in the white-crowned sparrow. Animal Behaviour, 32, 172–181. Beecher, M. D. 1996. Birdsong learning in the laboratory and field. In: Ecology and Evolution of Acoustic Communication in Birds (Ed. by D. E. Kroodsma & E. H. Miller), pp. 61–78. Ithaca, New York: Comstock. Brenowitz, E. A. 1997. Comparative approaches to the avian song system. Journal of Neurobiology, 33, 517–531. Burnell, K. & Rothstein, S. I. 1994. Variation in the structure of female brown-headed cowbird vocalizations and its relation to vocal function and development. Condor, 96, 703–715. Catchpole, C. K. & Slater, P. J. B. 1995. Bird Song: Biological Themes and Variations. New York: Cambridge University Press. Dufty, A. M. 1982. Movements and activities of radio-tracked brown-headed cowbirds. Auk, 99, 316–327. Dufty, A. M. 1985. Song sharing in the brown-headed cowbird (Molothrus ater). Zeitschrift fu¨r Tierpsychologie, 69, 177–190. Dufty, A. M., Jr & McChrystal, R. 1992. Vocalization and copulatory attempts in free-living brown-headed cowbirds. Journal of Field Ornithology, 63, 16–25. Dufty, A. M. & Wingfield, J. C. 1986a. Temporal patterns of circulating LH and steroid hormones in a brood parasite, the brown-headed cowbird, Molothrus ater. II. Females. Journal of Zoology, 208, 205–214. Dufty, A. M. & Wingfield, J. C. 1986b. Temporal patterns of circulating LH and steroid hormones in a brood parasite, the brown-headed cowbird, Molothrus ater. I. Males. Journal of Zoology, 208, 191–203. Fleischer, R. C. & Rothstein, S. I. 1988. Known secondary contact and rapid gene flow among subspecies and dialects in the brown-headed cowbird. Evolution, 42, 1146–1158. Fleischer, R. C., Smyth, A. P. & Rothstein, S. I. 1987. Temporal and age-related variation in the laying rate of the parasitic brownheaded cowbird in the eastern Sierra Nevada, California. Canadian Journal of Zoology, 65, 2724–2730. Friedmann, H. 1929. The Cowbirds, a Study in the Biology of Social Parasitism. Springfield, Illinois: C. C. Thomas. Friedmann, H. & Kiff, L. F. 1985. The parasitic cowbirds and their hosts. Proceedings of the Western Foundation of Vertebrate Zoology, 2, 225–304. Gorney-Labinger, E. 1997. Males sing while females choose: parallel development of male production and female recognition of two distinct song categories in brown-headed cowbirds. Ph.D. thesis. Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara.

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