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Nest-vicinity song exchanges may coordinate biparental care of northern cardinals
Anim. Behav., 1997, 54, 189–198
Nest-vicinity song exchanges may coordinate biparental care of northern cardinals SYLVIA L. HALKIN Department of Zoology, University of Wisconsin at Madison (Received 18 January 1995; initial acceptance 15 October 1995; final acceptance 11 October 1996; MS. number: 7230)
Abstract. In species with biparental care, communication between the parents may increase the efficiency and decrease the risks of care delivery. In northern cardinals, Cardinalis cardinalis, the female’s singing from the nest may provide information that allows her conspicuous mate to target his visits to the nest to times when food is needed, saving energy and flights that may attract nest predators. Thirteen pairs of cardinals were recorded in 25 nestings over six summers in Madison, Wisconsin, U.S.A. When a male with nestlings sang or called within 12 m of the nest, his probability of bringing food to the nest varied with his mate’s response. The male was more likely to come to the nest when the female sang than when she did not, unless she responded to the male’s song with a matching song type. Most males were least likely to come to the nest when their mates matched their songs. ?
Although biparental care is characteristic of birds, little is known about whether or how avian parents communicate to coordinate care delivery. In many passerine songbirds, the female incubates the eggs and broods the young nestlings; during the incubation and brooding periods, the male may be the primary provider of food at the nest. A female sitting on the nest may have more information than her mate about the need for food for herself and the nestlings. If she could share this information, her mate could avoid unnecessary and conspicuous trips to the nest. One way the female might signal her mate is by vocalizing from the nest. Females in a number of species vocalize from the nest (e.g. Armstrong 1973, pp. 167–170; Ritchison 1983; Inman 1986). Such vocalizing presumably makes the nest more conspicuous to predators and parasites (Armstrong 1973; Yasukawa 1989), and would not be expected to occur unless it confers sufficient benefits to offset this cost. Potential benefits The author received the Animal Behavior Society’s Allee award for outstanding doctoral research, on which this publication is based. Correspondence: S. L. Halkin, Department of Biological Sciences, Central Connecticut State University, New Britain, CT 06050-4010, U.S.A. (email: halkins@ ccsu.ctstateu.edu). 0003–3472/97/070189+10 $25.00/0/ar960415
1997 The Association for the Study of Animal Behaviour
may include teaching the young to recognize both parents’ vocalizations, thereby concentrating conspicuous begging on times when the parent is actually present (Hitchcock et al. 1989), facilitating parent–offspring recognition (e.g. Beecher et al. 1985) or family-group maintenance (Ritchison 1983) after the young fledge, selfstimulation of reproductive hormone output (Cheng 1992), promoting male vigilance for nest predators (Yasukawa 1989; McDonald & Greenberg 1991), or signalling the male to incubate the eggs (Armstrong 1973). The possibility that such vocalizations inform the male of the need for food at the nest has not been investigated. To test this possibility, I studied the vocal interactions of northern cardinals, Cardinalis cardinalis, in the vicinity of their nests. Anecdotal reports exist of female cardinals singing from the nest, sometimes followed by the male bringing food to the female (Wanamaker 1942; Laskey 1944; Kinser 1973; Stokes & Stokes 1983). Males provide a significant proportion of total food deliveries to nestling cardinals (Filliater & Breitwisch 1997; personal observation). In this study, I tested the hypothesis that female songs change the male’s probability of coming to the nest with food.
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190 METHODS
Study Area and Methods of Data Collection I recorded nesting cardinals during May– August, from 1981 to 1986, in a 25-ha peninsular nature reserve (Picnic Point) on the campus of the University of Wisconsin at Madison, U.S.A. Most nests were 1.5–2.0 m above the ground, in bushes or Eastern red cedars, Juniperus virginiana. I made observations and recordings from partially concealed locations under bushes or trees approximately 5 m from the nest. A Uher 4400 stereo tape-recorder was used with Uher M517 microphones mounted in Dan Gibson TM 45.7-cm parabolic reflectors. I simultaneously recorded the vocalizations of the male and female on separate channels: one microphone was pointed at the female on the nest, and the other was turned to track the male. I identified vocalizations from sonagrams made with either a Spectral Dynamics Corporation SD301D-C real time sound spectrum analyser or a Multigon Industries Uniscan II sound spectrum analyser. Thirteen cardinals were mist-netted and colourbanded for individual identification. Both mates were colour-banded in seven pairs (two pairs had the same male but different females). Only one of the pair was colour-banded in three pairs, and neither was banded in the remaining three pairs. I assumed that only one male and one female attended each nest, as was the case in the seven pairs in which both mates were banded. I also assumed that unbanded birds were recorded at only one nest; unlike the nests of the two simultaneously polygynous banded males, the nests of all unbanded birds appeared to be in different territories. If these assumptions are true, I recorded 22 individuals in 13 pairs. Banded pairs of cardinals in the study area occupied year-round territories. Typically, two of a pair’s three or four nesting attempts between May and September each produced one or more fledglings (personal observation). Incubation and brooding are performed only by the female (Laskey 1944; Bent 1968; personal observation). Incubation lasted 12–13 days. Nestlings remain in the nest for an additional 9–10 days, and the female spends most time brooding them during the first 4–7 days of nestling life (Bent 1968; personal observation). Males brought food to their mates during courtship and throughout the time the female was sitting on the nest, and I did
not see males visit the nest without food. Females also foraged for themselves, and both parents brought food to the nestlings. I recorded cardinals at 25 nests: nine pairs were recorded at one nest each, and the other four pairs were each recorded at 2–6 nests over 2–4 years. To obtain a data set that was not dominated by the few most frequently-recorded birds, I divided nests into two groups. The first group includes 10 ‘Independent’ nests, one from each of 10 pairs with non-overlapping membership. For birds recorded at more than one nest or with more than one mate, the nest with the largest number of recorded Interactions was used. The second group, analysed separately from the first, includes the remaining 15 ‘Repeat/re-mate’ nests. Of the Independent nests, I recorded seven during the egg period for 127.6 h and nine during the nestling period for 255.2 h. Total recording time at individual nests ranged from 5.4 to 29.7 h over 3–8 days during the egg period, and from 15.6 to 54.0 h over 4–7 days during the nestling period. Of the Repeat/re-mate nests, I recorded seven during the egg period for 63.7 h, and 14 during the nestling period for 235.7 h. I made all recordings between 0507 and 2058 hours. I present data for successive ‘Interactions’ between mates, delimited as follows. (1) An Interaction began either when the female was on the nest and the male first sang or called within 12 m (horizontal distance), or when the female sang or called from the nest and the male vocalized from within 12 m within the next minute. (2) An Interaction ended when the male came to the nest (regardless of whether vocalizations continued), when either mate moved more than 12 m from the nest, or when the male had been silent at an unknown distance from the nest for at least 1 min. I chose a 12-m radius around the nest because my previous observations indicated that females rarely sang when the male was more than 12 m from the nest; most singing by females began when the male was within 6–10 m. Vegetation almost always prevented mates from seeing one another at this distance. Males approached from more than 12 m away in fewer than 1% of all recordings of females singing from the nest. Singing by males more than 12 m from the nest appeared to be directed outside the territory (based on the male’s orientation and/or timing of singing relative to that of his neighbours).
Halkin: Nest-vicinity singing of cardinals
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Figure 1. (a) Sonagram of a single song, with component elements labelled. (b) A sequence of songs of the type shown in (a) sung by a male and female during the course of an Interaction. The female’s first song began during the sixth repetition of syllable type 2 in the male’s fourth song, and her second song began during the second repetition of syllable type 2 in the male’s fifth song. This Interaction lasted approximately 2 min, including a pause of 25 s between the male’s eighth and ninth songs. Recorded Interactions ranged from 1 s to almost 16 min (0–53 songs by males and 0–11 songs by females).
Several factors that varied between Interactions were disregarded in this study, either because I was unable to record them reliably or because they were too variable for me to obtain sample sizes adequate to determine whether they had an effect. These included whether the male was vocalizing immediately before he approached within 12 m of the nest, whether cardinals in other territories were singing or calling, how long the female had been on the nest, the number of eggs or young, and whether cowbird eggs or nestlings were present. There were no apparent differences in the male’s probability of visiting the nest when the female stayed on the nest versus left, so I combined these data. Identification of Songs, Song Subunits, and Song ‘Matching’ To understand comparisons of ways cardinals use song in Interactions, it is necessary to start
with information about the structure of cardinal songs. Unless otherwise noted, terminology in naming song subunits is from Lemon (1965), and I follow his criteria for defining these units. Cardinal songs consist of series of repeated component syllables (Figs 1, 2). Each syllable in turn consists of either a single continuous sonagraphic trace, or an ordered sequence of up to three such traces with different frequency distributions (subsyllables). I considered two syllables to be of the same type if their sonagrams were the same shape, within &250 Hz in overall frequency, and (with the exception of one atypically long syllable type) within &0.1 s in duration; previous authors have not quantified the measurements used to discriminate between syllable types. Apparent harmonics or non-harmonic spectrographic traces might be present or absent above the frequency with maximal energy (compare the second syllable types in the male’s and female’s songs in Fig. 2, row 2),
Animal Behaviour, 54, 1
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Figure 2. Sonagrams of all 18 syllable types used within 12 m of the nest in a complete sample of the songs recorded from one pair. The male’s and female’s renditions of the same syllable type are shown in the same row; one of the syllable types in row 8 was not recorded from the female in this pair, but was sung by other females. The female’s syllables in row 4, the male’s in row 8, and those of both sexes in row 9, are portions of songs; in all other cases whole songs are shown. Dashed vertical lines separate different syllable types within the same song. The two syllable types shown in the songs in row 5 were considered different because the first syllable type was consistently given with two subsyllables and the second was consistently given with three. The numbers of repetitions of each syllable type in a song varied widely; lengths of songs shown here are typical.
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Halkin: Nest-vicinity singing of cardinals 193
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and syllables were occasionally sung with one or two subsyllables missing (compare the first and second syllables in the male’s song in Fig. 2, row 6). These variations were generally ascribed to differences in recording volume or minor differences in rendition, and were not considered to be sufficient criteria for defining distinct syllable types. A song (‘utterance’ of Lemon 1965) is defined as a series of consecutive syllables separated from one another by silent intervals of less than 1 s; silent intervals of 1 s or longer separate consecutive songs (Lemon 1965). Songs are composed of syllables of one or more types. A song type is defined by its constituent syllable types and the order in which they are given. In series of consecutive songs, cardinals often alternate between longer songs with two syllable types and shorter songs with just the first of those syllable types (Lemon & Chatfield 1971; personal observation). In my study area, each syllable type is usually given in combination with only one other syllable type, and the order in which they are sung is generally fixed (Halkin 1990). After a number of renditions of songs that start in the same way, males giving territorial song switch to another set of songs that start with a different syllable type (Lemon & Chatfield 1971; Ritchison 1988; personal observation). The grouping and somewhat interchangeable use of songs with shared syllable types suggests that syllable-type sharing is an important way in which cardinals categorize songs, and was the basis of my decision to define songs as ‘matching’ if they shared at least one of their component syllable types (Fig. 1b). Cardinals rarely switched between song types with unshared syllable types during the course of an Interaction. Because changes in motivation (and signal) might occur during the course of an Interaction, however, I scored matching only on the last song of each mate that followed a song of the other. Use of Non-song Vocalizations Cardinals use ‘chips’ as general-purpose contact calls (Lemon 1968b; Stokes & Stokes 1983; sonagrams in Lemon 1968b; Halkin 1990). Chip calls were used in a variety of different contexts in nest-vicinity Interactions. Chip calls given by themselves were sometimes the male’s only vocalizations in an Interaction, but they were also commonly given between his songs. Chip calls by
females were principally associated with their own approach to or departure from the nest. Females occasionally gave chip calls at other points during both Interactions in which the male came to the nest and those in which he stayed away; although not investigated here, it is possible that chip calls were used differently in Interactions with the two different outcomes. If the male approached to within 1 m of the nest, one or both mates commonly gave low-amplitude versions of chips, as well as calls fitting the description of the ‘tooks’ that Shaver and Roberts (1933, page 118) reported from females (sonagrams in Halkin 1990). Since a male within 1 m of the nest almost always proceeded to the nest itself, there is not enough variability in outcome to test whether vocalizations influenced his probability of coming to the nest at this point. Hypothesis Testing I compared the male’s probability of visiting the nest after different kinds of vocal Interactions between the male and female. Initial male vocalizations (defined as occurring before the first song of the female, if she sang) were categorized on the basis of whether the male sang. For each of these categories (initial male vocalizations consisting of only chip calls, and initial male vocalizations consisting of either songs or a combination of songs and chips), I compared the male’s probability of visiting the nest when the female sang and when she did not sing. If both mates sang, I compared Interactions in which they sang matching songs (as defined above) to Interactions in which they sang songs that did not match. I also briefly examined the use of specific individual song types and the significance of switching between song types. Vocal Interactions between mates occur relatively infrequently, so sample sizes in this study are necessarily small. Averaged over the time during which I recorded them, pairs ranged from 0.86 to 3.7 Interactions/h during incubation, and 0.4 to 3.9 Interactions/h during the nestling period. When possible, I present separate data for each pair to present an accurate picture of variation among pairs. When sample sizes are small and pairs do not show obvious variation, however, I sometimes discuss data combined from different pairs. I give data and statistical tests for the Independent nests. In all cases, parallel analyses were
Halkin: Nest-vicinity singing of cardinals
RESULTS Song Repertoires Used in Interactions Although many authors have stated that male and female cardinals sing the same songs (e.g. Lemon 1968a; Ritchison 1986), the complete syllable-type repertoire of a female has not previously been published. I present here complete syllable-type repertoires used within 12 m of the nest by one pair of cardinals (Fig. 2); all 18 syllable types shown were used by most males and females in my study area; only one cardinal used additional syllable types (two, used by one female). Syllable-type repertoires of individuals were judged to have been fully sampled when days or weeks of additional recordings did not reveal any new syllable types. Comparisons of the Male’s Probability of Visiting the Nest after Different Kinds of Vocal Interactions Nestling period When the male’s initial vocalizations were calls, he was more likely to come to the nest if the female sang than if she did not sing (Fig. 3; Wilcoxon matched-pairs test, T=2, N=7 nests with both kinds of Interactions and differing proportions of male visits in the two kinds of Interactions, two-tailed P=0.05). Among the 88 Interactions in which the female sang (top graph, Fig. 3), the male did not sing after the female in 60; he came to the nest in 47 (78%) of these. The male sang songs that did not match the female’s in 22 Interactions, and came to the nest in 16 (73%) of these. The male sang songs that matched the female’s in the remaining six Interactions, and came to the nest in three (50%) of these. When the male’s initial vocalizations included songs, his subsequent probability of coming to the nest appeared to differ depending upon whether the female matched his songs (Fig. 4). Seven males
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performed for the Repeat/re-mate nests, and unless otherwise noted, parallel results were found. To compare the proportion of male visits to the nest in different kinds of vocal Interactions, I calculated for each nest the following proportion: number of Interactions in which the male came to the nest/total number of Interactions. Unless otherwise noted, these proportions are the data on which statistical tests were performed.
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came to the nest in higher proportions of Interactions when the female sang non-matching songs than when she did not sing (Fig. 4). Five of the seven males with data to compare came to the nest in lower proportions of Interactions when their mates matched their songs than when the female did not sing (Fig. 4). The proportion of male visits can be compared for all three types of Interactions (female matched, female sang and did not match and female did not sing) with a non-parametric two-way analysis of variance procedure using ranks of observed proportions that have been ‘aligned’ by subtracting from each of the observed proportions the mean proportion of male visits for that pair (Lehman & D’Abrera 1975, pp. 270–273). This comparison just misses statistical significance at the P=0.05 level (Q | 2 =5.781; the critical value for significance at P=0.05 is 5.99). These trends were also present in the Repeat/ re-mate nests, but were less strong. The male’s vocalizations did not appear to predict his behaviour. Comparison of the male’s
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Pair Figure 4. Comparisons of males’ probabilities of coming to each of nine nests during the nestling period, based on the female’s response when initial male vocalizations included song.
probability of coming to the nest in Interactions that eliminate the possible influence of the female’s song (bottom graphs, Figs 3, 4) shows that five males visited the nest in a higher proportion of Interactions when they just called, and four visited more often when their vocalizations included song. I briefly considered two other aspects of singing behaviour: the use of specific individual syllable or song types, and switching between song types. All song and syllable types in Fig. 2 were used in Interactions both when males came to the nest and when they stayed away. Sample sizes were not sufficiently large, however, to judge whether the male came to the nest in different proportions of Interactions based on which song or syllable types were used.
To test whether switching between song types was correlated with the male’s probability of coming to the nest, I chose two Independent nestings (those of pair 3 and pair 9) that provided sample sizes sufficient to assess switching by both sexes. During Interactions, birds switched song types between songs that shared syllable types and, more rarely, between songs that did not share syllable types. Both females did both kinds of switching, and both males did the first kind only. Neither male’s probability of coming to the nest varied between Interactions with and without switching of either type by either sex (all Ps>0.48, two-tailed Fisher’s exact probability tests comparing numbers of Interactions in which the male came to the nest versus stayed away, in Interactions with versus without switching). Egg period Males rarely visited the nest while the female was incubating eggs, and females rarely sang from the nest. Of the 228 Interactions recorded at seven Independent nests with incubating females, the male’s initial vocalizations were calls in 56. The female sang in eight of these, and the male came to the nest in two (25%) of the eight. The female did not sing in the remaining 48 Interactions, and the male came to the nest in 11 (23%) of them. The male’s initial vocalizations included songs in 172 Interactions. The female responded with matching song in 20 of these, and the male came to the nest in one (5%) of the 20. The female responded with songs that did not match in 15 Interactions; the male did not come to the nest in any of the 15. The female did not sing in the remaining 137 Interactions, and the male came to the nest in six (4%) of these. DISCUSSION During the nestling period, the male’s probability of coming to the nest varied with his mate’s singing behaviour, supporting the hypothesis that female songs provide information to the male about the need for food at the nest. When the male initially called, he came to the nest more often if the female sang than if she did not. When the male’s initial vocalizations included song, most males came to the nest most often if the female responded with a non-matching song, next most often if she did not sing at all, and least often
Halkin: Nest-vicinity singing of cardinals if she responded with a matching song, although sample sizes of Interactions with matching are small. The female thus appears to be able to signal the male to come to the nest, whether his vocalizations are calls or songs. Song matching by the female appears to signal a singing male to stay away; I have not identified an analogous signal used by the female when the male is not singing. The male did not always come to the nest when the female sang after he called, or when she sang songs that did not match his songs. The male may not always have food to bring to the nest when he vocalizes within 12 m, and in this case the female’s signals may just tell him that he needs to forage. Conversely, a male may sometimes come to the nest in spite of the female’s matching his song to leave food with her rather than keeping it in his own crop, even if food is not needed immediately at the nest. Song matching when the male stays away from the nest has an intriguing parallel in song communication between territorial males and may be conveying the specific message ‘stay away from where I am’ in both contexts (J. Baylis, personal communication). Cardinals (Lemon 1968a) and Carolina wrens, Thryothorus ludovicianus (Simpson 1985), show increased song matching as singing male neighbours approach shared territory boundaries; in great tits, Parus major, increased song matching correlates with other measures of response to playbacks, and Krebs et al. (1981) suggested that matching may be a graded signal indicating probability of escalated fighting. Morton (1982) believed that song matching may help birds exchange accurate information on the distance between them, and as such may be used as a threat during confrontations at territory boundaries. In the context of nest-vicinity song exchanges, accurate information about the female’s location could serve to assure a male that is not going to visit the nest that his mate is present at the nest and caring for the young or eggs. During the egg period, the rare songs of incubating females appear to have little if any effect on the male’s probability of coming to the nest. Instead, unlike during the nestling period, the male’s calling without song may be the best indication of his infrequent visits: males came to the nest proportionately more often when they just called than when they sang, regardless of singing by the female.
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The differences in the relative numbers of Interactions with male and female song during the egg and nestling periods are consistent with likely differences in the functions and risks of song during these periods. Females may have less need to signal the male during the egg period because food need not yet be brought for nestlings. Female song carries a particular risk because it is generally given from the nest itself, and decreasing the length of time over which it is given would help to reduce the probability of nest parasitism (in early incubation) and predation. Non-visiting males may more often sing during the egg period to stimulate aspects of the female’s reproductive and parental behaviour associated with the early nesting period (e.g. Brockway 1965; Hinde & Steel 1976; Kroodsma 1976). This study suggests that communication may be important in coordinating biparental care, and that signalling previously assumed to function only broadly in maintaining contact or pair bonding between mates, in announcing the arrival of a parent with food, or in teaching offspring to recognize their parents, may actually convey different specific messages about care provision. Although male cardinals’ conspicuous coloration may have provided particularly strong selection pressures favouring the development of a communication system that allows them to avoid unnecessary visits to the nest, such communication systems may exist in other species of birds that vocalize from their nests. In addition to communication associated with bringing food to the young, it may be profitable to investigate vocalizations associated with one mate taking the place of the other on the nest during incubation or brooding (e.g. Howes-Jones 1985; Ritchison (1983) listed seven species in which females sing in the context of nest exchanges). In both nest exchanges and coordination of parental feeding visits, birds may need to convey similar information about whether their mates should come to the nest. ACKNOWLEDGMENTS I thank Jeffrey Baylis for ideas, advice and guidance at all stages of the research and writing. Jack P. Hailman, Charles Snowdon, Edward Beals and Stanley Temple also provided helpful direction. Ann Marie Francis, Jeffrey Baylis, Catherine Young, Mark Fulton, Daniel Wallace, John Havel, Theodore Halkin, Emile DeVito, Douglas
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Levey, W. John Haynes and Richard Smith each provided much-appreciated occasional assistance in the field. Comments by Michael Beecher, Donald Kroodsma, Ken Yasukawa, Luis Baptista, Meredith West, Jeffrey Baylis, David Spector, Daniel Halkin, Emilia Martins, Matt Lee, L. LaReesa Wolfenbarger and anonymous referees led to considerable improvements in the manuscript. Kenneth Olesen, Richard Gange, David Hoffman, Dirk Wilker, Jerold Bialzik, Sooil Kim, Regina Dardzienski, Cheryle Hughes and Donald Chandler helped with equipment and illustrations. Daniel Miller provided statistical advice. I thank Barbara Simpson, Robert Lemon, Russell Charif and faculty and graduate students at the University of Wisconsin at Madison for useful discussions. This research was supported by a National Science Foundation Graduate Fellowship, the Frank M. Chapman Fund of the American Museum of Natural History, the Friends of the University of Wisconsin at Madison Arboretum and the University of Wisconsin at Madison Department of Zoology. REFERENCES Armstrong, E. A. 1973. A Study of Bird Song. New York: Dover. Beecher, M. D., Stoddard, P. K. & Loesche, P. 1985. Recognition of parents’ voices by young cliff swallows. Auk, 102, 600–605. Bent, A. C. 1968. Richmondena cardinalis cardinalis (Linnaeus), Eastern cardinal. In: Life Histories of North American Cardinals, Grosbeaks, Buntings, Towhees, Finches, Sparrows, and Allies (Ed. by A. C. Bent), pp. 1–15. Washington, D.C.: Smithsonian Institution Press. Brockway, B. F. 1965. Stimulation of ovarian development and egg laying by male courtship vocalizations in budgerigars, Melopsittacus undulatus. Anim. Behav., 13, 575–578. Cheng, M.-F. 1992. For whom does the female dove coo? A case for the role of vocal self-stimulation. Anim. Behav., 43, 1035–1044. Filliater, T. S. & Breitwisch, R. B. 1997. Nestling provisioning by the extremely dichromatic northern cardinal. Wilson Bull., 109, 145–153 Halkin, S. L. 1990. Singing from the nest: intrapair communication in cardinals. Ph.D. thesis, University of Wisconsin at Madison. Hinde, R. A. & Steel, E. 1976. The effect of male song on an estrogen-dependent behavior pattern in the female canary, Serinus canarius. Horm. Behav., 7, 293–304. Hitchcock, R. R., Mirarchi, R. E. & Lishak, R. S. 1989. Recognition of individual male parent vocalizations by nestling mourning doves. Anim. Behav., 37, 517– 520.
Howes-Jones, D. 1985. Relationships among song activity, context, and social behavior in the warbling vireo. Wilson Bull., 97, 4–20. Inman, B. L. 1986. Female vocalizations and their role in the avian breeding cycle. Ann. N. Y. Acad. Sci., 474, 44–52. Kinser, G. W., Jr. 1973. Ecology and behavior of the cardinal, Richmondena cardinalis (L), in southern Indiana. Ph.D. thesis, Indiana University. Krebs, J. R., Ashcroft, R. & Van Orsdol, K. 1981. Song matching in the great tit, Parus major. Anim. Behav., 29, 918–923. Kroodsma, D. E. 1976. Reproductive development in a female songbird: differential stimulation by quality of male song. Science, 192, 574–575. Laskey, A. R. 1944. A study of the cardinal in Tennessee. Wilson Bull., 56, 27–44. Lehman, E. H. & D’Abrera, H. J. M. 1975. Nonparametrics: Statistical Methods Based on Ranks. Oakland, California: Holden-Day. Lemon, R. E. 1965. The song repertoires of cardinals (Richmondena cardinalis) at London, Ontario. Can. J. Zool., 43, 559–569. Lemon, R. E. 1968a. The relation between organization and function of song in cardinals. Behaviour, 32, 158–178. Lemon, R. E. 1968b. The displays and call notes of cardinals. Can. J. Zool., 46, 141–151. Lemon, R. E. & Chatfield, C. 1971. Organization of song in cardinals. Anim. Behav., 19, 1–17. McDonald, M. V. & Greenberg, R. 1991. Nest departure calls in female songbirds. Condor, 93, 365–373. Morton, E. S. 1982. Grading, discreteness, redundancy, and motivation-structural rules. In: Acoustic Communication in Birds, Vol. 1: Production, Perception, and Design Features of Sounds (Ed. by D. E. Kroodsma & E. H. Miller), pp. 183–212. New York: Academic Press. Ritchison, G. 1983. The function of singing in female black-headed grosbeaks (Pheucticus melanocephalus): family-group maintenance. Auk, 100, 105–116. Ritchison, G. 1986. The singing behavior of female northern cardinals. Condor, 88, 156–159. Ritchison, G. 1988. Song repertoires and the singing behavior of male northern cardinals. Wilson Bull., 100, 583–603. Shaver, J. M. & Roberts, M. B. 1933. A brief study of the courtship of the eastern cardinal. J. Tenn. Acad. Sci., 8, 116–123. Simpson, B. S. 1985. Effects of location in territory and distance from neighbours on the use of song repertoires by Carolina wrens. Anim. Behav., 33, 793–804. Stokes, D. W. & Stokes, L. Q. 1983. Northern cardinal, Cardinalis cardinalis. In: A Guide to Bird Behavior, Vol. II, pp. 246–257. Boston: Little, Brown and Company. Wanamaker, J. F. 1942. A study of the courtship and nesting of the eastern cardinal, Richmondena c. cardinalis (Linnaeus). M.S. thesis, Cornell University. Yasukawa, K. 1989. The costs and benefits of a vocal signal: the nest-associated ‘chit’ of the female redwinged blackbird, Agelaius phoeniceus. Anim. Behav., 38, 866–874.
Nest-vicinity song exchanges may coordinate biparental care of northern cardinals SYLVIA L. HALKIN Department of Zoology, University of Wisconsin at Madison (Received 18 January 1995; initial acceptance 15 October 1995; final acceptance 11 October 1996; MS. number: 7230)
Abstract. In species with biparental care, communication between the parents may increase the efficiency and decrease the risks of care delivery. In northern cardinals, Cardinalis cardinalis, the female’s singing from the nest may provide information that allows her conspicuous mate to target his visits to the nest to times when food is needed, saving energy and flights that may attract nest predators. Thirteen pairs of cardinals were recorded in 25 nestings over six summers in Madison, Wisconsin, U.S.A. When a male with nestlings sang or called within 12 m of the nest, his probability of bringing food to the nest varied with his mate’s response. The male was more likely to come to the nest when the female sang than when she did not, unless she responded to the male’s song with a matching song type. Most males were least likely to come to the nest when their mates matched their songs. ?
Although biparental care is characteristic of birds, little is known about whether or how avian parents communicate to coordinate care delivery. In many passerine songbirds, the female incubates the eggs and broods the young nestlings; during the incubation and brooding periods, the male may be the primary provider of food at the nest. A female sitting on the nest may have more information than her mate about the need for food for herself and the nestlings. If she could share this information, her mate could avoid unnecessary and conspicuous trips to the nest. One way the female might signal her mate is by vocalizing from the nest. Females in a number of species vocalize from the nest (e.g. Armstrong 1973, pp. 167–170; Ritchison 1983; Inman 1986). Such vocalizing presumably makes the nest more conspicuous to predators and parasites (Armstrong 1973; Yasukawa 1989), and would not be expected to occur unless it confers sufficient benefits to offset this cost. Potential benefits The author received the Animal Behavior Society’s Allee award for outstanding doctoral research, on which this publication is based. Correspondence: S. L. Halkin, Department of Biological Sciences, Central Connecticut State University, New Britain, CT 06050-4010, U.S.A. (email: halkins@ ccsu.ctstateu.edu). 0003–3472/97/070189+10 $25.00/0/ar960415
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may include teaching the young to recognize both parents’ vocalizations, thereby concentrating conspicuous begging on times when the parent is actually present (Hitchcock et al. 1989), facilitating parent–offspring recognition (e.g. Beecher et al. 1985) or family-group maintenance (Ritchison 1983) after the young fledge, selfstimulation of reproductive hormone output (Cheng 1992), promoting male vigilance for nest predators (Yasukawa 1989; McDonald & Greenberg 1991), or signalling the male to incubate the eggs (Armstrong 1973). The possibility that such vocalizations inform the male of the need for food at the nest has not been investigated. To test this possibility, I studied the vocal interactions of northern cardinals, Cardinalis cardinalis, in the vicinity of their nests. Anecdotal reports exist of female cardinals singing from the nest, sometimes followed by the male bringing food to the female (Wanamaker 1942; Laskey 1944; Kinser 1973; Stokes & Stokes 1983). Males provide a significant proportion of total food deliveries to nestling cardinals (Filliater & Breitwisch 1997; personal observation). In this study, I tested the hypothesis that female songs change the male’s probability of coming to the nest with food.
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Study Area and Methods of Data Collection I recorded nesting cardinals during May– August, from 1981 to 1986, in a 25-ha peninsular nature reserve (Picnic Point) on the campus of the University of Wisconsin at Madison, U.S.A. Most nests were 1.5–2.0 m above the ground, in bushes or Eastern red cedars, Juniperus virginiana. I made observations and recordings from partially concealed locations under bushes or trees approximately 5 m from the nest. A Uher 4400 stereo tape-recorder was used with Uher M517 microphones mounted in Dan Gibson TM 45.7-cm parabolic reflectors. I simultaneously recorded the vocalizations of the male and female on separate channels: one microphone was pointed at the female on the nest, and the other was turned to track the male. I identified vocalizations from sonagrams made with either a Spectral Dynamics Corporation SD301D-C real time sound spectrum analyser or a Multigon Industries Uniscan II sound spectrum analyser. Thirteen cardinals were mist-netted and colourbanded for individual identification. Both mates were colour-banded in seven pairs (two pairs had the same male but different females). Only one of the pair was colour-banded in three pairs, and neither was banded in the remaining three pairs. I assumed that only one male and one female attended each nest, as was the case in the seven pairs in which both mates were banded. I also assumed that unbanded birds were recorded at only one nest; unlike the nests of the two simultaneously polygynous banded males, the nests of all unbanded birds appeared to be in different territories. If these assumptions are true, I recorded 22 individuals in 13 pairs. Banded pairs of cardinals in the study area occupied year-round territories. Typically, two of a pair’s three or four nesting attempts between May and September each produced one or more fledglings (personal observation). Incubation and brooding are performed only by the female (Laskey 1944; Bent 1968; personal observation). Incubation lasted 12–13 days. Nestlings remain in the nest for an additional 9–10 days, and the female spends most time brooding them during the first 4–7 days of nestling life (Bent 1968; personal observation). Males brought food to their mates during courtship and throughout the time the female was sitting on the nest, and I did
not see males visit the nest without food. Females also foraged for themselves, and both parents brought food to the nestlings. I recorded cardinals at 25 nests: nine pairs were recorded at one nest each, and the other four pairs were each recorded at 2–6 nests over 2–4 years. To obtain a data set that was not dominated by the few most frequently-recorded birds, I divided nests into two groups. The first group includes 10 ‘Independent’ nests, one from each of 10 pairs with non-overlapping membership. For birds recorded at more than one nest or with more than one mate, the nest with the largest number of recorded Interactions was used. The second group, analysed separately from the first, includes the remaining 15 ‘Repeat/re-mate’ nests. Of the Independent nests, I recorded seven during the egg period for 127.6 h and nine during the nestling period for 255.2 h. Total recording time at individual nests ranged from 5.4 to 29.7 h over 3–8 days during the egg period, and from 15.6 to 54.0 h over 4–7 days during the nestling period. Of the Repeat/re-mate nests, I recorded seven during the egg period for 63.7 h, and 14 during the nestling period for 235.7 h. I made all recordings between 0507 and 2058 hours. I present data for successive ‘Interactions’ between mates, delimited as follows. (1) An Interaction began either when the female was on the nest and the male first sang or called within 12 m (horizontal distance), or when the female sang or called from the nest and the male vocalized from within 12 m within the next minute. (2) An Interaction ended when the male came to the nest (regardless of whether vocalizations continued), when either mate moved more than 12 m from the nest, or when the male had been silent at an unknown distance from the nest for at least 1 min. I chose a 12-m radius around the nest because my previous observations indicated that females rarely sang when the male was more than 12 m from the nest; most singing by females began when the male was within 6–10 m. Vegetation almost always prevented mates from seeing one another at this distance. Males approached from more than 12 m away in fewer than 1% of all recordings of females singing from the nest. Singing by males more than 12 m from the nest appeared to be directed outside the territory (based on the male’s orientation and/or timing of singing relative to that of his neighbours).
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Figure 1. (a) Sonagram of a single song, with component elements labelled. (b) A sequence of songs of the type shown in (a) sung by a male and female during the course of an Interaction. The female’s first song began during the sixth repetition of syllable type 2 in the male’s fourth song, and her second song began during the second repetition of syllable type 2 in the male’s fifth song. This Interaction lasted approximately 2 min, including a pause of 25 s between the male’s eighth and ninth songs. Recorded Interactions ranged from 1 s to almost 16 min (0–53 songs by males and 0–11 songs by females).
Several factors that varied between Interactions were disregarded in this study, either because I was unable to record them reliably or because they were too variable for me to obtain sample sizes adequate to determine whether they had an effect. These included whether the male was vocalizing immediately before he approached within 12 m of the nest, whether cardinals in other territories were singing or calling, how long the female had been on the nest, the number of eggs or young, and whether cowbird eggs or nestlings were present. There were no apparent differences in the male’s probability of visiting the nest when the female stayed on the nest versus left, so I combined these data. Identification of Songs, Song Subunits, and Song ‘Matching’ To understand comparisons of ways cardinals use song in Interactions, it is necessary to start
with information about the structure of cardinal songs. Unless otherwise noted, terminology in naming song subunits is from Lemon (1965), and I follow his criteria for defining these units. Cardinal songs consist of series of repeated component syllables (Figs 1, 2). Each syllable in turn consists of either a single continuous sonagraphic trace, or an ordered sequence of up to three such traces with different frequency distributions (subsyllables). I considered two syllables to be of the same type if their sonagrams were the same shape, within &250 Hz in overall frequency, and (with the exception of one atypically long syllable type) within &0.1 s in duration; previous authors have not quantified the measurements used to discriminate between syllable types. Apparent harmonics or non-harmonic spectrographic traces might be present or absent above the frequency with maximal energy (compare the second syllable types in the male’s and female’s songs in Fig. 2, row 2),
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Figure 2. Sonagrams of all 18 syllable types used within 12 m of the nest in a complete sample of the songs recorded from one pair. The male’s and female’s renditions of the same syllable type are shown in the same row; one of the syllable types in row 8 was not recorded from the female in this pair, but was sung by other females. The female’s syllables in row 4, the male’s in row 8, and those of both sexes in row 9, are portions of songs; in all other cases whole songs are shown. Dashed vertical lines separate different syllable types within the same song. The two syllable types shown in the songs in row 5 were considered different because the first syllable type was consistently given with two subsyllables and the second was consistently given with three. The numbers of repetitions of each syllable type in a song varied widely; lengths of songs shown here are typical.
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and syllables were occasionally sung with one or two subsyllables missing (compare the first and second syllables in the male’s song in Fig. 2, row 6). These variations were generally ascribed to differences in recording volume or minor differences in rendition, and were not considered to be sufficient criteria for defining distinct syllable types. A song (‘utterance’ of Lemon 1965) is defined as a series of consecutive syllables separated from one another by silent intervals of less than 1 s; silent intervals of 1 s or longer separate consecutive songs (Lemon 1965). Songs are composed of syllables of one or more types. A song type is defined by its constituent syllable types and the order in which they are given. In series of consecutive songs, cardinals often alternate between longer songs with two syllable types and shorter songs with just the first of those syllable types (Lemon & Chatfield 1971; personal observation). In my study area, each syllable type is usually given in combination with only one other syllable type, and the order in which they are sung is generally fixed (Halkin 1990). After a number of renditions of songs that start in the same way, males giving territorial song switch to another set of songs that start with a different syllable type (Lemon & Chatfield 1971; Ritchison 1988; personal observation). The grouping and somewhat interchangeable use of songs with shared syllable types suggests that syllable-type sharing is an important way in which cardinals categorize songs, and was the basis of my decision to define songs as ‘matching’ if they shared at least one of their component syllable types (Fig. 1b). Cardinals rarely switched between song types with unshared syllable types during the course of an Interaction. Because changes in motivation (and signal) might occur during the course of an Interaction, however, I scored matching only on the last song of each mate that followed a song of the other. Use of Non-song Vocalizations Cardinals use ‘chips’ as general-purpose contact calls (Lemon 1968b; Stokes & Stokes 1983; sonagrams in Lemon 1968b; Halkin 1990). Chip calls were used in a variety of different contexts in nest-vicinity Interactions. Chip calls given by themselves were sometimes the male’s only vocalizations in an Interaction, but they were also commonly given between his songs. Chip calls by
females were principally associated with their own approach to or departure from the nest. Females occasionally gave chip calls at other points during both Interactions in which the male came to the nest and those in which he stayed away; although not investigated here, it is possible that chip calls were used differently in Interactions with the two different outcomes. If the male approached to within 1 m of the nest, one or both mates commonly gave low-amplitude versions of chips, as well as calls fitting the description of the ‘tooks’ that Shaver and Roberts (1933, page 118) reported from females (sonagrams in Halkin 1990). Since a male within 1 m of the nest almost always proceeded to the nest itself, there is not enough variability in outcome to test whether vocalizations influenced his probability of coming to the nest at this point. Hypothesis Testing I compared the male’s probability of visiting the nest after different kinds of vocal Interactions between the male and female. Initial male vocalizations (defined as occurring before the first song of the female, if she sang) were categorized on the basis of whether the male sang. For each of these categories (initial male vocalizations consisting of only chip calls, and initial male vocalizations consisting of either songs or a combination of songs and chips), I compared the male’s probability of visiting the nest when the female sang and when she did not sing. If both mates sang, I compared Interactions in which they sang matching songs (as defined above) to Interactions in which they sang songs that did not match. I also briefly examined the use of specific individual song types and the significance of switching between song types. Vocal Interactions between mates occur relatively infrequently, so sample sizes in this study are necessarily small. Averaged over the time during which I recorded them, pairs ranged from 0.86 to 3.7 Interactions/h during incubation, and 0.4 to 3.9 Interactions/h during the nestling period. When possible, I present separate data for each pair to present an accurate picture of variation among pairs. When sample sizes are small and pairs do not show obvious variation, however, I sometimes discuss data combined from different pairs. I give data and statistical tests for the Independent nests. In all cases, parallel analyses were
Halkin: Nest-vicinity singing of cardinals
RESULTS Song Repertoires Used in Interactions Although many authors have stated that male and female cardinals sing the same songs (e.g. Lemon 1968a; Ritchison 1986), the complete syllable-type repertoire of a female has not previously been published. I present here complete syllable-type repertoires used within 12 m of the nest by one pair of cardinals (Fig. 2); all 18 syllable types shown were used by most males and females in my study area; only one cardinal used additional syllable types (two, used by one female). Syllable-type repertoires of individuals were judged to have been fully sampled when days or weeks of additional recordings did not reveal any new syllable types. Comparisons of the Male’s Probability of Visiting the Nest after Different Kinds of Vocal Interactions Nestling period When the male’s initial vocalizations were calls, he was more likely to come to the nest if the female sang than if she did not sing (Fig. 3; Wilcoxon matched-pairs test, T=2, N=7 nests with both kinds of Interactions and differing proportions of male visits in the two kinds of Interactions, two-tailed P=0.05). Among the 88 Interactions in which the female sang (top graph, Fig. 3), the male did not sing after the female in 60; he came to the nest in 47 (78%) of these. The male sang songs that did not match the female’s in 22 Interactions, and came to the nest in 16 (73%) of these. The male sang songs that matched the female’s in the remaining six Interactions, and came to the nest in three (50%) of these. When the male’s initial vocalizations included songs, his subsequent probability of coming to the nest appeared to differ depending upon whether the female matched his songs (Fig. 4). Seven males
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performed for the Repeat/re-mate nests, and unless otherwise noted, parallel results were found. To compare the proportion of male visits to the nest in different kinds of vocal Interactions, I calculated for each nest the following proportion: number of Interactions in which the male came to the nest/total number of Interactions. Unless otherwise noted, these proportions are the data on which statistical tests were performed.
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came to the nest in higher proportions of Interactions when the female sang non-matching songs than when she did not sing (Fig. 4). Five of the seven males with data to compare came to the nest in lower proportions of Interactions when their mates matched their songs than when the female did not sing (Fig. 4). The proportion of male visits can be compared for all three types of Interactions (female matched, female sang and did not match and female did not sing) with a non-parametric two-way analysis of variance procedure using ranks of observed proportions that have been ‘aligned’ by subtracting from each of the observed proportions the mean proportion of male visits for that pair (Lehman & D’Abrera 1975, pp. 270–273). This comparison just misses statistical significance at the P=0.05 level (Q | 2 =5.781; the critical value for significance at P=0.05 is 5.99). These trends were also present in the Repeat/ re-mate nests, but were less strong. The male’s vocalizations did not appear to predict his behaviour. Comparison of the male’s
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probability of coming to the nest in Interactions that eliminate the possible influence of the female’s song (bottom graphs, Figs 3, 4) shows that five males visited the nest in a higher proportion of Interactions when they just called, and four visited more often when their vocalizations included song. I briefly considered two other aspects of singing behaviour: the use of specific individual syllable or song types, and switching between song types. All song and syllable types in Fig. 2 were used in Interactions both when males came to the nest and when they stayed away. Sample sizes were not sufficiently large, however, to judge whether the male came to the nest in different proportions of Interactions based on which song or syllable types were used.
To test whether switching between song types was correlated with the male’s probability of coming to the nest, I chose two Independent nestings (those of pair 3 and pair 9) that provided sample sizes sufficient to assess switching by both sexes. During Interactions, birds switched song types between songs that shared syllable types and, more rarely, between songs that did not share syllable types. Both females did both kinds of switching, and both males did the first kind only. Neither male’s probability of coming to the nest varied between Interactions with and without switching of either type by either sex (all Ps>0.48, two-tailed Fisher’s exact probability tests comparing numbers of Interactions in which the male came to the nest versus stayed away, in Interactions with versus without switching). Egg period Males rarely visited the nest while the female was incubating eggs, and females rarely sang from the nest. Of the 228 Interactions recorded at seven Independent nests with incubating females, the male’s initial vocalizations were calls in 56. The female sang in eight of these, and the male came to the nest in two (25%) of the eight. The female did not sing in the remaining 48 Interactions, and the male came to the nest in 11 (23%) of them. The male’s initial vocalizations included songs in 172 Interactions. The female responded with matching song in 20 of these, and the male came to the nest in one (5%) of the 20. The female responded with songs that did not match in 15 Interactions; the male did not come to the nest in any of the 15. The female did not sing in the remaining 137 Interactions, and the male came to the nest in six (4%) of these. DISCUSSION During the nestling period, the male’s probability of coming to the nest varied with his mate’s singing behaviour, supporting the hypothesis that female songs provide information to the male about the need for food at the nest. When the male initially called, he came to the nest more often if the female sang than if she did not. When the male’s initial vocalizations included song, most males came to the nest most often if the female responded with a non-matching song, next most often if she did not sing at all, and least often
Halkin: Nest-vicinity singing of cardinals if she responded with a matching song, although sample sizes of Interactions with matching are small. The female thus appears to be able to signal the male to come to the nest, whether his vocalizations are calls or songs. Song matching by the female appears to signal a singing male to stay away; I have not identified an analogous signal used by the female when the male is not singing. The male did not always come to the nest when the female sang after he called, or when she sang songs that did not match his songs. The male may not always have food to bring to the nest when he vocalizes within 12 m, and in this case the female’s signals may just tell him that he needs to forage. Conversely, a male may sometimes come to the nest in spite of the female’s matching his song to leave food with her rather than keeping it in his own crop, even if food is not needed immediately at the nest. Song matching when the male stays away from the nest has an intriguing parallel in song communication between territorial males and may be conveying the specific message ‘stay away from where I am’ in both contexts (J. Baylis, personal communication). Cardinals (Lemon 1968a) and Carolina wrens, Thryothorus ludovicianus (Simpson 1985), show increased song matching as singing male neighbours approach shared territory boundaries; in great tits, Parus major, increased song matching correlates with other measures of response to playbacks, and Krebs et al. (1981) suggested that matching may be a graded signal indicating probability of escalated fighting. Morton (1982) believed that song matching may help birds exchange accurate information on the distance between them, and as such may be used as a threat during confrontations at territory boundaries. In the context of nest-vicinity song exchanges, accurate information about the female’s location could serve to assure a male that is not going to visit the nest that his mate is present at the nest and caring for the young or eggs. During the egg period, the rare songs of incubating females appear to have little if any effect on the male’s probability of coming to the nest. Instead, unlike during the nestling period, the male’s calling without song may be the best indication of his infrequent visits: males came to the nest proportionately more often when they just called than when they sang, regardless of singing by the female.
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The differences in the relative numbers of Interactions with male and female song during the egg and nestling periods are consistent with likely differences in the functions and risks of song during these periods. Females may have less need to signal the male during the egg period because food need not yet be brought for nestlings. Female song carries a particular risk because it is generally given from the nest itself, and decreasing the length of time over which it is given would help to reduce the probability of nest parasitism (in early incubation) and predation. Non-visiting males may more often sing during the egg period to stimulate aspects of the female’s reproductive and parental behaviour associated with the early nesting period (e.g. Brockway 1965; Hinde & Steel 1976; Kroodsma 1976). This study suggests that communication may be important in coordinating biparental care, and that signalling previously assumed to function only broadly in maintaining contact or pair bonding between mates, in announcing the arrival of a parent with food, or in teaching offspring to recognize their parents, may actually convey different specific messages about care provision. Although male cardinals’ conspicuous coloration may have provided particularly strong selection pressures favouring the development of a communication system that allows them to avoid unnecessary visits to the nest, such communication systems may exist in other species of birds that vocalize from their nests. In addition to communication associated with bringing food to the young, it may be profitable to investigate vocalizations associated with one mate taking the place of the other on the nest during incubation or brooding (e.g. Howes-Jones 1985; Ritchison (1983) listed seven species in which females sing in the context of nest exchanges). In both nest exchanges and coordination of parental feeding visits, birds may need to convey similar information about whether their mates should come to the nest. ACKNOWLEDGMENTS I thank Jeffrey Baylis for ideas, advice and guidance at all stages of the research and writing. Jack P. Hailman, Charles Snowdon, Edward Beals and Stanley Temple also provided helpful direction. Ann Marie Francis, Jeffrey Baylis, Catherine Young, Mark Fulton, Daniel Wallace, John Havel, Theodore Halkin, Emile DeVito, Douglas
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Levey, W. John Haynes and Richard Smith each provided much-appreciated occasional assistance in the field. Comments by Michael Beecher, Donald Kroodsma, Ken Yasukawa, Luis Baptista, Meredith West, Jeffrey Baylis, David Spector, Daniel Halkin, Emilia Martins, Matt Lee, L. LaReesa Wolfenbarger and anonymous referees led to considerable improvements in the manuscript. Kenneth Olesen, Richard Gange, David Hoffman, Dirk Wilker, Jerold Bialzik, Sooil Kim, Regina Dardzienski, Cheryle Hughes and Donald Chandler helped with equipment and illustrations. Daniel Miller provided statistical advice. I thank Barbara Simpson, Robert Lemon, Russell Charif and faculty and graduate students at the University of Wisconsin at Madison for useful discussions. This research was supported by a National Science Foundation Graduate Fellowship, the Frank M. Chapman Fund of the American Museum of Natural History, the Friends of the University of Wisconsin at Madison Arboretum and the University of Wisconsin at Madison Department of Zoology. REFERENCES Armstrong, E. A. 1973. A Study of Bird Song. New York: Dover. Beecher, M. D., Stoddard, P. K. & Loesche, P. 1985. Recognition of parents’ voices by young cliff swallows. Auk, 102, 600–605. Bent, A. C. 1968. Richmondena cardinalis cardinalis (Linnaeus), Eastern cardinal. In: Life Histories of North American Cardinals, Grosbeaks, Buntings, Towhees, Finches, Sparrows, and Allies (Ed. by A. C. Bent), pp. 1–15. Washington, D.C.: Smithsonian Institution Press. Brockway, B. F. 1965. Stimulation of ovarian development and egg laying by male courtship vocalizations in budgerigars, Melopsittacus undulatus. Anim. Behav., 13, 575–578. Cheng, M.-F. 1992. For whom does the female dove coo? A case for the role of vocal self-stimulation. Anim. Behav., 43, 1035–1044. Filliater, T. S. & Breitwisch, R. B. 1997. Nestling provisioning by the extremely dichromatic northern cardinal. Wilson Bull., 109, 145–153 Halkin, S. L. 1990. Singing from the nest: intrapair communication in cardinals. Ph.D. thesis, University of Wisconsin at Madison. Hinde, R. A. & Steel, E. 1976. The effect of male song on an estrogen-dependent behavior pattern in the female canary, Serinus canarius. Horm. Behav., 7, 293–304. Hitchcock, R. R., Mirarchi, R. E. & Lishak, R. S. 1989. Recognition of individual male parent vocalizations by nestling mourning doves. Anim. Behav., 37, 517– 520.
Howes-Jones, D. 1985. Relationships among song activity, context, and social behavior in the warbling vireo. Wilson Bull., 97, 4–20. Inman, B. L. 1986. Female vocalizations and their role in the avian breeding cycle. Ann. N. Y. Acad. Sci., 474, 44–52. Kinser, G. W., Jr. 1973. Ecology and behavior of the cardinal, Richmondena cardinalis (L), in southern Indiana. Ph.D. thesis, Indiana University. Krebs, J. R., Ashcroft, R. & Van Orsdol, K. 1981. Song matching in the great tit, Parus major. Anim. Behav., 29, 918–923. Kroodsma, D. E. 1976. Reproductive development in a female songbird: differential stimulation by quality of male song. Science, 192, 574–575. Laskey, A. R. 1944. A study of the cardinal in Tennessee. Wilson Bull., 56, 27–44. Lehman, E. H. & D’Abrera, H. J. M. 1975. Nonparametrics: Statistical Methods Based on Ranks. Oakland, California: Holden-Day. Lemon, R. E. 1965. The song repertoires of cardinals (Richmondena cardinalis) at London, Ontario. Can. J. Zool., 43, 559–569. Lemon, R. E. 1968a. The relation between organization and function of song in cardinals. Behaviour, 32, 158–178. Lemon, R. E. 1968b. The displays and call notes of cardinals. Can. J. Zool., 46, 141–151. Lemon, R. E. & Chatfield, C. 1971. Organization of song in cardinals. Anim. Behav., 19, 1–17. McDonald, M. V. & Greenberg, R. 1991. Nest departure calls in female songbirds. Condor, 93, 365–373. Morton, E. S. 1982. Grading, discreteness, redundancy, and motivation-structural rules. In: Acoustic Communication in Birds, Vol. 1: Production, Perception, and Design Features of Sounds (Ed. by D. E. Kroodsma & E. H. Miller), pp. 183–212. New York: Academic Press. Ritchison, G. 1983. The function of singing in female black-headed grosbeaks (Pheucticus melanocephalus): family-group maintenance. Auk, 100, 105–116. Ritchison, G. 1986. The singing behavior of female northern cardinals. Condor, 88, 156–159. Ritchison, G. 1988. Song repertoires and the singing behavior of male northern cardinals. Wilson Bull., 100, 583–603. Shaver, J. M. & Roberts, M. B. 1933. A brief study of the courtship of the eastern cardinal. J. Tenn. Acad. Sci., 8, 116–123. Simpson, B. S. 1985. Effects of location in territory and distance from neighbours on the use of song repertoires by Carolina wrens. Anim. Behav., 33, 793–804. Stokes, D. W. & Stokes, L. Q. 1983. Northern cardinal, Cardinalis cardinalis. In: A Guide to Bird Behavior, Vol. II, pp. 246–257. Boston: Little, Brown and Company. Wanamaker, J. F. 1942. A study of the courtship and nesting of the eastern cardinal, Richmondena c. cardinalis (Linnaeus). M.S. thesis, Cornell University. Yasukawa, K. 1989. The costs and benefits of a vocal signal: the nest-associated ‘chit’ of the female redwinged blackbird, Agelaius phoeniceus. Anim. Behav., 38, 866–874.