Song and Mate Choice in : How the Development of Behavior Helps Us Understand Author(s): Stephen Nowicki and William A. Searcy Reviewed work(s): Source: The Auk, Vol. 122, No. 1 (Jan., 2005), pp. 1-14 Published by: University of California Press on behalf of the American Ornithologists' Union Stable URL: http://www.jstor.org/stable/4090344 . Accessed: 06/04/2012 11:51

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

University of California Press and American Ornithologists' Union are collaborating with JSTOR to digitize, preserve and extend access to The Auk.

http://www.jstor.org |TheAuk e l A Quarterly Journalof I , Vol. 122 No. 1 January 2005

The Auk 122(1):1-14, 2005 ? The American Ornithologists' Union, 2005. Printed in USA. PERSPECTIVESIN ORNITHOLOGY SONG AND MATE CHOICE IN BIRDS: HOW THE DEVELOPMENT OF BEHAVIOR HELPS US UNDERSTAND FUNCTION

STEPHEN NOWICKI1'3 AND WILLIAM A. SEARCY2 'Department of , Duke University, Durham, North Carolina 27708, USA; and 2Department of Biology, University of Miami, Coral Gables, Florida 33124, USA

AMONG HIS MANY contributions to the study to the more contemporary disciplines of neu- of behavior, Nobel laureate Niko roethology, which focuses primarily on causal Tinbergen is perhaps best remembered for ar- mechanisms, and behavioral , which ticulating the 'four questions" of , out- emphasizes functional and evolutionary analy- lining four ways in which one could answer the ses. Recently, however, new reasons for interest broader question of "why" an animal behaves in development have emerged, as researchers the way it does (Tinbergen 1951, 1963). Those have realized that developmental processes, four questions address (1) causation (i.e. what interacting with neural and physiological physiological mechanisms are responsible for mechanisms of causation, can have important the expression of the behavior?), (2) ontogeny consequences for the function and (what factors affect the development of the be- of behavior. Nowhere is the interaction of havior?), (3) function (how does the behavior development and causation with the function enhance ?), and (4) evolution (what are and evolution of behavior more apparent than the historical antecedents of the behavior?). in the study of song. Here, we explore the Although researchers may focus their work value of the interplay among Tinbergen's four on only one or a subset of those questions, questions for understanding a central question Tinbergen maintained that all four must be ad- about bird song. dressed to answer completely the question of "why" an animal performs a behavior. DEVELOPMENT AND NEUROBIOLOGY OP BIRD SONG Tinbergen credited (1942) with introducing the idea that causal, functional, Bird song provides an exception to the gen- and historical analyses represent distinct ap- eralization that behavioral development was proaches to the study of behavior. Tinbergen's relatively neglected in the period between own contribution, he claimed, was to add Tinbergen's day and the present. Largely ontogeny to Huxley's list (Tinbergen 1963). through the work of Peter Marler and his col- Thus, it is ironic that interest in developmient leagues, bird song became the single most waned, to some degree, as the science of ethol- important model system for studying the de- ogy that Tinbergen helped establish gave rise velopment of behavior. Although most of that work was not directed specifically at functional questions, many of the findings turn out to have 3E-mail:[email protected] functional implications. The basic picture that

1 2 Perspectivesin Ornithology [Auk, Vol. 122

emerged is that song in oscines is learned by of HVC, for example, has been shown to be pos- young birds through listening to older birds itively associated with measures of song reper- sing. Males isolated at an early age to prevent toire size, both in between- comparisons through imitation subsequently pro- (DeVoogd et al. 1993, Szekely et al. 1996) and in duce songs that are abnormalin many features comparisons between individuals within spe- (Thorpe 1958, Marler 1970). Tutoring using cies (Nottebohm et al. 1981, Airey and DeVoogd tape-recordedsongs (Marler1970) or live tutors 2000, Airey et al. 2000). Exceptions to that rela- (Baptista and Petrinovich 1984) is sufficient to tionship have also been noted, however (Kirn et enable hand-reared males to develop normal al. 1989, Brenowitz et al. 1991). The size of HVC songs. In the absence of any social cues, hand- and RA change seasonally; in Song Sparrows reared males show a preference for learning (Melospiza melodia), the change corresponds to conspecific over heterospecific songs (Thorpe seasonal changes in note stereotypy, such that 1958, Marler and Peters 1977). In some species, notes are less stereotyped when HVC and RA memorization of song models is concentrated volumes are low (Smith et al. 1997). within a limited "criticallearning period," often roughly 20 to 60 days after hatching (Marler FUNCTIONAL ASPECTS OF SONG: FEMALE CHOICE and Peters 1987, 1988), though social and other OF MATE factors may modify the timing (Baptista and Petrinovich1986, Petrinovich and Baptista1987, In general, a male bird's song has two pri- Nelson 1998). Birds deafened after their critical mary audiences (Searcy and Andersson 1986, learning period but before their own song has Catchpole and Slater 1995). To conspecific crystallized produce songs that are even more males, song serves as a "keep out" signal, ad- abnormal than those of isolate males (Konishi vertising the presence of a territorial male and 1965), which implies that, to shape their songs repelling potential intruders from the space he to match the models they have learned, males is defending. Experimental evidence for that must listen to their own production. function comes from studies in which male With the discovery that song is controlled birds are surgically muted and subsequently by a relatively well-defined series of discrete experience difficulty in maintaining their terri- nuclei (Nottebohm et al. 1976), song also tories (Peek 1972, Smith 1979, McDonald 1989). became a major model system for the study of Further evidence comes from studies in which the neural control of behavior in vertebrates males are removed entirely from their territo- (Konishi et al. 1989). The "song system" of os- ries and replaced by loudspeakers that either cines is organized in two pathways (Mooney do or do not broadcast song; territories remain 1999). The motor pathway includes the nuclei free from intruders for a longer time with play- HVC and RA. Lesion of either of those nuclei back than without (Goransson et al. 1974, Krebs impairs an adult's ability to sing (Nottebohm et 1977, Yasukawa 1981, Falls 1988, Nowicki et al. al. 1976), which indicates that they are impor- 1998b). tant in storage and production of song. The an- Although those experiments demonstrate terior forebrainpathway includes Area X, DLM, that song functions as a keep-out signal against and IMAN, with Area X receiving input from other males, the designs they have used have not HVC and 1MAN projecting to RA. Lesions of proved efficient for determining what features Area X or IMAN impair song learning in young of song are important for that function (Searcy birds, which suggests that the anteriorforebrain and Nowicki 2000). We know much more about pathway plays an important role in acquisition the relationship between form and function and development of song (Bottjeret al. 1984, with respect to the second major function of Sohrabjiet al. 1990). Development of the song song, that of attracting and stimulating females. system has been described in a few species of The best evidence that females are attracted to oscines and has been found to largely coincide song has come from experimental studies with with the memorization phase of song develop- cavity-nesting species, in which unoccupied ment (Bottjeret al. 1985, Nordeen and Nordeen nest boxes were outfitted with loudspeakers. 1988, Nordeen et al. 1989, Nowicki et al. 1998a). Boxes from which songs were played were in- The size of some of the nuclei has been demon- spected or occupied by females more quickly strated to have functional implications. Volume than boxes where the loudspeaker remained January2005] Perspectivesin Ornithology 3 silent (Eriksson and Wallin 1986, Mountjoy and individual male produces. In general, females Lemon 1991, Johnson and Searcy 1996). The ef- are more attracted to and more likely to mate fect of song on female reproductive behavior is with males that have larger repertoires or sing demonstrated by laboratory studies showing more complex songs (Catchpole 1980; Searcy that females increase nest building activity and 1984; Catchpole et al. 1984, 1986; Hasselquist et when exposed to song (Hinde al. 1996; Reid et al. 2004). The third dimension and Steel 1976, Kroodsma 1976, Searcy and of song variation commonly affecting female Marler 1981) and by field studies showing that response is the amount a male sings, or a male's females lay their clutches earlier the more their "song output," with females preferring males mate sings (Wright and Cuthill 1992). that sing longer songs or longer song bouts, sing It is not hard to envision how selection would at a faster rate, and so forth (Gottlander 1987, favor female response to conspecific male song Alatalo et al. 1990, Eens et al. 1991, Wasserman if song only serves to identify the location of a and Cigliano 1991, Kempenaers et al. 1997). potential mate: a female has to find at least one male of the correct species and mate with him WHY SHOULD FEMALE BIRDS PREFER CERTAIN to have any reproductive success at all. Much SONG TRAITS TO OTHERS? ethological work took that point of view and thus focused on the question of how species- It is in addressing the question of why female distinctiveness is encoded in song (e.g. Emlen show the song preferences they do 1972, Becker 1982). But different males of the that the interaction among the development, same species usually do not all sing the same neurobiology, and function of song becomes way, and the strength of a female's response important. Preference for a particular song to song-or a female's song "preference"- characteristic will evolve if females receive depends on the way a particular male sings. In some benefit from with a male whose other words, female birds not only use song to songs exhibit that characteristic (Andersson find a conspecific male, they also use song to 1994). Therefore, preferences for song traits discriminate among males as they choose mates. may evolve if those traits are reliable indicators The question of why females show preferences of some aspect of male quality that benefits the for specific attributes of male displays such as female. For a signal to serve as an indicator trait song has been a central problem in behavioral in the context of mate choice, variation in its ecology (Andersson 1994). expression must correspond reliably with some Although there is almost immeasurable va- aspect of signaler quality, such as condition or riety in the way different species of birds sing viability. Because signalers can benefit in that and how songs vary within a species, three context from exaggerating their quality, a sig- categories of variation appear to have the most naling system can be maintained only if the reli- consistent effects on female response across ability of the signal is somehow ensured (Searcy different species (Searcy and Nowicki 2000, and Nowicki 2005). Nowicki et al. 2002a). Geographic differences One mechanism for ensuring the reliability of represent the most ubiquitous kind of varia- signals of quality is expressed by the handicap tion affecting female response. In some species, principle (Zahavi 1975, 1977), which states that there is marked variation in song across very signals are reliable because they are costly. Both short distances, with distinct boundaries defin- the cost and the effectiveness of the signal are ing local "dialects" (Marler and Tamura 1962, assumed to increase with signaling level. If the McGregor 1980); in other species, geographic cost of a given signaling level is higher for sig- variation is more subtle and gradual, with dif- nalers of low quality than for signalers of high ferences becoming apparent only over a con- quality, then the optimal signaling level is lower siderable distance (Searcy et al. 2002). In both for the low-quality signaler than for the high- cases, females generally prefer local songs to quality signaler (Grafen 1990a, Johnstone 1997). songs produced by males from distant popula- Under those assumptions, all signalers exhibit tions (Searcy 1992a). A second kind of variation the level of signaling that is in their own best that commonly affects female response is song interests, and yet the signal is still reliable. complexity, typically measured as the number An indicator trait may correlate with some as- of different song types or syllable types an pect of a male's phenotype that directly increases 4 Perspectives in Ornithology [Auk, Vol. 122 the reproductive success of the female with That hypothesis also has difficulties as a gen- which he mates, such as his ability to defend a eral explanation, however. One difficulty is that , deter predators, provide parental care, males in at least some species learn their songs and so forth. An indicator also may correlate after dispersing, making the dialect a male sings with some aspect of a male's genetic quality, a poor marker of his natal (Baptista which will benefit females with which he mates and Morton 1988). Another difficulty is that in by providing their offspring with "good " species with continuous and gradual geographic that affect their viability and future reproduc- differences in song, typical dispersal distances tive success. Theoretical models demonstrate are such that it is unlikely a female would ever that female preference for a trait can evolve if encounter a male producing a song outside of females obtain indirect benefits by mating with the range she would accept as a normal local genotypically superior males (Andersson 1986, dialect (Searcy et al. 2002). A third difficulty is Pomiankowski 1987, Iwasa et al. 1991), and can that little evidence exists that mating with a con- also evolve if females obtain only direct benefits specific male from outside the local population by mating with phenotypically superior males would actually be disadvantageous in birds or (Heywood 1989, Hoelzer 1989, Grafen 1990b). other (Pusey and 1996). The handicap mechanism provides an obvi- Two additional hypotheses that could explain ous explanation for female preferences based the evolution of female preferences for a signal on song output: the relevant costs stem from without requiring the signal to be costly are the effects of singing on the singer's the Fisher mechanism and sensory bias. In the balance. Measurements of oxygen consump- Fisher mechanism, a female preference becomes tion during singing indicate that the energy genetically correlated with the preferred trait, costs of song are remarkably low (Oberweger and both become exaggerated in a runaway and Goller 2001; Ward et al. 2003, 2004). Other process (Fisher 1930, Andersson 1994). Song at- studies have shown, however, that provisioning tributes that vary geographically do not exhibit of males in the field has a strong positive effect the exaggeration predicted by that hypothesis; on their singing rates (Searcy 1979, Davies and but song complexity, in some cases, arguably Lundberg 1984, Gottlander 1987). Thus, despite does. Thus, the Fisher mechanism might ex- its low energy cost, singing must have a nega- plain female preferences for song complexity, tive effect on energy balance, perhaps because though some theoreticians have argued that it time spent singing reduces time available for should be a hypothesis of last resort (Grafen foraging. The negative effect of singing on 1990a). The sensory bias hypothesis suggests energy balance provides a cost to song output that female preferences for male display traits that explains its reliability with regard to a male are nonadaptive consequences of attributes of attribute that females might well be interested female perceptual or neurobiological mecha- in-the present condition of the male. nisms that are adaptive in other contexts (Ryan Costs are not so easy to assign to the other and Rand 1993, Ryan 1998). The sensory bias categories of song traits preferred by females. hypothesis is unlikely to explain preferences for Time and energy costs of singing a diverse rep- geographic variants, given the reciprocal ertoire of song or syllable types should be no of such preferences. Although it has been sug- greater than those of repeating single song or gested to explain female preferences for larger syllable types. Similarly, singing local variants repertoires (Searcy 1992b, Collins 1999), the sen- of song cannot be consistently more expensive sory bias hypothesis is not supported by histori- in time and energy than singing foreign vari- cal evidence (Gray and Hagelin 1996). . Alternative hypotheses exist, however, We have proposed instead that female pref- that explain female preferences on the basis of erences based on complexity and geographic complexity and geography without invoking origin of song can be explained by the handicap costs. One such hypothesis, which accounts principle, but with reliability enforced by de- only for preferences based on geographic origin, velopmental costs rather than production costs suggests that females benefit by mating with (Nowicki et al. 1998a, Nowicki and Searcy 2004). local males because those males carry alleles It is in this "developmental stress" hypothesis that are better adapted to the local environment that the interplay of development, neurobiol- (Nottebohm 1972, Baker and Cunningham 1985). ogy, and function comes into focus. January 2005] Perspectivesin Ornithology 5

THE DEVELOPMENTAL STRESS HYPOTHESIS effects that parallel those of direct nutritional deprivation. Exposure to cold temperatures may We have already seen that song learning, stor- also have parallel effects. Such considerations age, and production are controlled in songbirds have led to a consensus that the "nutritional by a series of discrete brain structures and that stress hypothesis" should be broadened to a "de- those structures develop, in large part, during velopmental stress hypothesis" (Buchanan et al. the first few months post-hatching. In Zebra 2003, Nowicki and Searcy 2004) to acknowledge (Taenopygiaguttata), for example, RA and the potential importance of sources of stress HVC increase in size between 10 and 50 days other than nutritional deprivation. after hatching (Bottjer et al. 1985, Konishi and The developmental stress hypothesis leads to Akutagawa 1985, Nordeen and Nordeen 1988), a number of testable predictions. One obvious whereas the pathways connecting them develop prediction is that stress experienced soon after between 15 and 35 days after hatching (Mooney hatching will have lasting effects on develop- and Rao 1994). Timing of development of those ment of the song system in the brain. Nowicki et structures is similar or just slightly later in al. (2002a) tested that prediction by manipulat- Common Canaries (Serinus canaria; Nottebohm ing in hand-reared Swamp Sparrows et al. 1986, Alvarez-Buyalla et al. 1994) and during the period when they would normally Swamp Sparrows (M. georgiana; Nordeen et al. be dependent on their parents for food. A 1989). Nowicki et al. (1998a) pointed out that the well-fed group was provided with unlimited period just after hatching, when the song system amounts of hand-rearing diet while a nutrition- is developing and forming neural connections, ally restricted group was limited to 70% of what is also a period in which young songbirds are the well-fed birds consumed. were ex- particularly vulnerable to nutritional stress, first amined when the birds reached adulthood. The because of their dependence on their parents to well-fed subjects had HVC volumes -30% larger provide food, and later because of their own in- and RA volumes -45% larger than the nutrition- experience as foragers. Because the young bird's ally restricted birds. Those differences can be general phenotype is developing rapidly during explained, in part, by an effect of nutrition on the same period, males are faced with a trade-off overall telencephalon volume, which was 15% between investment in their song system and greater in the well-fed group. In addition, the investment in other aspects of their phenotype. ratio of RA volume to overall telencephalon In such a situation, animals are expected to volume was significantly greater in the well-fed give priority to investment in traits that affect group than in the nutritionally restricted birds, survival over investment in traits important in showing that RA, at least, was differentially display (Andersson 1986). The song system may affected by stress. Buchanan et al. (2004) have thus be among the first traits sacrificed if a young shown a similar effect of developmental stress experiences nutritional stress. Song, on song-system nuclei in Zebra Finches; in that and especially learned features of song, therefore case, there appeared to be a differential effect of becomes a sensitive indicator of a male's history stress on HVC volume. of nutritional stress and of the male's ability to A second prediction is that developmental withstand the effects of stress. Because song is stress will affect song features, including fea- thus an indicator of male quality, females are tures that are important to female preferences. selected to prefer mating with males that have In a correlational field study, Nowicki et al. superior songs. (2000) showed that the rate of feather growth in In the above formulation, we have emphasized nestling Great Reed Warblers (Acrocephalusarun- the potential effect of nutritional stress on song dinaceus) was positively associated with their development, following Nowicki et al. (1998a) syllable repertoire sizes as adults. Therefore, a in their original statement of what they termed large repertoire produced by an adult male in- the "nutritional stress hypothesis." Buchanan et dicates that he grew well when young. Evidence al. (2003), however, have pointed out that other from both laboratory experiments (Catchpole et types of stresses can have similar effects on both al. 1986) and field correlations (Hasselquist et song development and phenotypic development. al. 1996, Hasselquist 1998) indicate that female Parasites, for example, can drain nutritional Great Reed Warblers prefer males that have resources away from growth, and thus have large syllable repertoires. 6 Perspectives in Ornithology [Auk, Vol. 122

This second prediction has also been tested song: males stressed by either food deprivation experimentally in a series of studies. One or corticosterone administration developed such study is the manipulation of nutrition in shorter songs with fewer syllables and lower hand-reared Swamp Sparrows described above peak frequencies than controls. Female Zebra (Nowicki et al. 2002a). In that experiment, well- Finches have been shown to prefer long songs fed males did not develop larger song reper- over short ones in laboratory tests (Clayton and toires than nutritionally restricted ones. Well- Prove 1989)-again, developmental stresses fed males did, however, learn their tutor songs change song in a direction less preferred by significantly more accurately, as measured by females. spectrogram cross-correlations between model A third prediction of the developmental notes and learned copies. It is not known wheth- stress hypothesis is that males subjected to er female Swamp Sparrows prefer well-learned stress during early development will possess songs, but there is evidence of such a preference inferior phenotypes as adults, with some of in their congener, the Song Sparrow. Hand- that inferiority in traits important to the fitness reared male Song Sparrows were tutored with of their mates. Although this seems a logical songs from a local population in Pennsylvania. expectation, few direct tests have been made. Adult females from the same population subse- Searcy et al. (2004) manipulated nutrition in quently showed a preference for those songs of hand-reared Song Sparrows, using methods the hand-reared males that were accurate cop- similar to those previously employed in Swamp ies of the tutor songs over songs that were poor Sparrows (Nowicki et al. 2002a). Nutritionally copies (Nowicki et al. 2002b). restricted Song Sparrows grew more slowly Buchanan et al. (2003) tested the effects of when young and were still significantly smaller a rather different nutritional manipulation in body size as adults. Studies of other species on song development in European Starlings of birds have also found that restricting food (Sturnus vulgaris). Between the ages of roughly provided to nestlings reduces their growth, 40 and 120 days, control birds were given un- with effects that may or may not persist into interrupted access to food while experimental adulthood (Richner et al. 1989, Lacombe et birds were deprived of food each day for a al. 1994). Adult females prefer larger males as randomly chosen 4-h period. The treatment mates in some bird species but not in others had a counterintuitive effect on body mass, (Schluter and Smith 1986, Weatherhead and with the experimental birds maintaining higher Boag 1995). Early developmental stresses might average mass than the controls through most of be expected to affect more subtle aspects of the the treatment period. Nevertheless, intermit- phenotype, such as immunocompetence and lo- tent food deprivation had a negative effect on comotor performance, but little is known about song development: deprived birds sang signifi- such effects in birds. cantly shorter songs (Buchanan et al. 2003) and Although testing of the developmental stress produced a significantly smaller repertoire of hypothesis is still in its early days, the hypoth- phrase types (Spencer et al. 2004). Song length esis has already received considerable support. and repertoire size are typically correlated with It appears that early developmental stresses one another in European Starlings, and both are that might be expected to impair development positively associated with female mating pref- of the overall phenotype also affect song devel- erences (Eens et al. 1991, Mountjoy and Lemon opment, and that the effects are in directions 1996). that make the song less preferred by conspecific Spencer et al. (2003) manipulated nutrition in females. There is also support for the idea that young Zebra Finches by limiting the amount of the effects of stress on song are mediated by food available to parents to feed their young be- effects on development of the song system in tween the ages of 5 and 30 days post-hatching. the brain. Much remains to be investigated; in A second treatment group was stressed, not by particular, a large of song variables has food deprivation but by daily doses of corticos- hardly been touched on, either with respect terone. The latter treatment mimics a general- to the effects of developmental stress or with ized stress, given that corticosterone is released respect to functional considerations in general. in birds in response to various types of stresses. That class of song variables can be termed "vo- The two stress treatments had similar effects on cal performance." January 2005] Perspectivesin Ornithology 7

VOCAL PERFORMANCE, FEMALE PREFERENCES, AND the maximum bandwidth. Those considerations DEVELOPMENTAL STRESS produce an upper limit to bandwidth that decreases as syllable repetition rate increases. When critics evaluate an opera singer, the cri- Evidence for the reality of that upper limit teria that we have so far applied to bird song are comes from the distribution of frequency band- relatively unimportant. Repertoire size might widths and syllable rates between and within be weighed a little, output less, and geographic species of emberizids (Podos 1997, Ballentine et origin not at all. Instead, the singer is likely al. 2004); those distributions are triangular, such to be assessed on traits such as vocal range that no songs have both the highest bandwidths (the range of frequencies produced), dynam- and the highest syllable rates. ics (the ability to increase and decrease sound The upper limit of bandwidth and rate de- intensity), intonation (the ability to achieve a fines a performance limit; males producing desired pitch with precision), vibrato (produc- songs close to the limit may be said to have tion of a tremulous effect through slight and high vocal performance, and those producing rapid changes in pitch), and so forth. All those songs far from the limit have low vocal per- criteria are concerned with how well the singer formance (Podos 2001). Once we can measure performs in aspects of singing that are physi- vocal performance, we can test whether females cally difficult; we can categorize such criteria prefer high performance to low. Ballentine et as measures of "vocal performance." It would al. (2004) performed such a test with Swamp seem logical that vocal performance might also Sparrows, using the distribution of bandwidth be important in birds and, in particular, that and syllable rates in the species' songs to define female birds might judge prospective mates its performance limit. They then tested female on performance features as well as on the traits Swamp Sparrows for response to pairs of songs, we have already discussed. Attention has only one near the upper limit and one farther from recently been turned to that possibility, perhaps it. Females showed a consistent preference for because of the difficulty of determining what songs near the upper limit-that is, for the sorts of feats are physically difficult for birds to songs of higher vocal performance. perform when singing. Below, we discuss what Common Canaries provide a related example is known thus far about female choice for vocal of a female preference based on vocal perfor- performance and then speculate about possible mance. Vallet and Kreutzer (1995) found that application of the developmental stress hypoth- female Common Canaries prefer a particular esis to performance features. phrase , labeled an "A" phrase, over other The case that currently provides the best in- types of phrases found in male song. "'A"phras- sight into what makes songs difficult for birds to es are characterized by the rapid repetition of perform involves a trade-off between frequency syllables containing two, frequency-modu- bandwidth and syllable repetition rate. To pro- lated notes. When presented with a range of duce a high-frequency sound, a male songbird "A" phrases, female Common Canaries are opens its beak wide, which effectively shortens especially responsive to those with the highest the vocal tract and raises its resonance fre- repetition rates (Vallet et al. 1998). Those results quency. To produce a low-frequency sound, the suggest that female canaries attend to the same male closes its bill, effectively lengthening the kind of performance limit operating in em- vocal tract and lowering its resonance frequency berizids-that is, a limit on the speed at which (Nowicki 1987; Westneat et al. 1993; Podos et al. syllables of high bandwidth can be repeated. 1995, 2004; Hoese et al. 2000). To produce a sylla- To test that possibility, Draganoiu et al. (2002) ble encompassing a wide range of frequencies - presented females with syllables of different that is, with a wide frequency bandwidth-the bandwidths, with either normal or artificially bird must open and close its bill over a wide elevated repetition rates. Females responded angle. If syllables are produced at a low rate, most strongly to syllables that combined high enough time is available per syllable to allow a bandwidth with elevated repetition rate. Again, large angle of movement and thus a large band- the evidence supports a female preference for width; as the syllable repetition rate increases, high vocal performance. however, the time per syllable decreases, and The existence of female preferences based on so must the maximum angle of movement and vocal performance leads to the familiar question 8 Perspectives in Ornithology [Auk, Vol. 122 of how females might benefit from such prefer- Whether the index argument is ever the best ex- ence. In the case of performance cues, the usual planation for signal reliability is a question we answer seems particularly appealing: that fe- discuss in detail elsewhere (Searcy and Nowicki males benefit from preferring the display trait 2005). in question because it is a reliable indicator of Application of the developmental stress hy- male quality. That answer is appealing for per- pothesis to vocal performance is, at this point, formance measures because of the argument, speculative; we can adduce no evidence sup- made by Maynard Smith and Harper (2003), porting the hypothesis with respect to perfor- that the reliability of performance-based signals mance features. The hypothesis can, however, is inevitable and needs no special and onerous be tested in the context of vocal performance explanation like that provided by the handicap just as it has been tested for other song features: principle. Maynard Smith and Harper (1995, by manipulating the environment of develop- 2003) classify signals of that type as "index" ment and observing effects on aspects of vocal signals, which they equate with Enquist's (1985) performance. A valuable adjunct of such experi- "performance-based" signals, and which they ments would be to study the anatomical and define as signals "whose intensity is causally re- physiological properties that change along with lated to the quality being signalled, and which performance features, so that we can begin to cannot be faked." They give as examples of understand the physical and physiological basis index signals the courtship dance of Drosophila of vocal performance. suboscura and the display flights of fritillary but- terflies (Maynard Smith and Harper 2003). The CONCLUSION idea is that the performance of those signals is so intimately tied to the qualities that the re- Asking why female birds respond to song the ceivers are interested in that exaggeration is not way they do illustrates the enduring value of possible, and the signals are perforce reliable. Tinbergen's "four questions," and at the same The index argument is not so straightforward time generates a new appreciation for the cen- with respect to song performance, however. tral role of the second of those questions, that Presumably, a female bird benefits from assess- concerning ontogeny. Ontogeny is important to ing aspects of male quality, such as parental song function because of the role of develop- ability or heritable viability. We know relatively mental costs in enforcing signal reliability. The little about the structures that affect a male's idea that developmental costs are important song performance, but presumably they might to maintaining reliability is not new, but such include the song nuclei in the brain, the nerves costs have usually been ascribed only to signals innervating the syrinx, the syringeal muscles, that depend on large and obviously expensive and so forth. The point is that the quality of the anatomical structures, such as antlers in latter structures does not directly affect parental or long tails in birds. Here, we have argued ability or male viability, and so the tie between that developmental costs can also be important male quality and song performance is not a di- for understanding the function and evolution rect one. A male could, in theory, invest in high of complex behaviors such as bird song, even song performance without investing in parental though no exaggerated external structures are ability and viability, though that course may involved. never be advantageous in practice. We therefore The assumption that song has important argue that the reliability of song performance as developmental costs is supported by what a cue to male quality is best explained by de- we know about the neurological structures velopmental costs, specifically by the trade-off responsible for song learning and production between investment in the structures leading and about the development of those structures. to superior song performance and in whatever Especially important is that the timing of song- aspects of the phenotype contribute to male system development overlaps both with growth parental ability, high viability, and the like. Put and maturation and with periods of extraordi- another way, we believe that the reliability of nary stress in a young bird's . That overlap song performance as an indicator of male qual- forces a developmental trade-off that can re- ity is better explained by the developmental veal a male's phenotypic and genetic quality. stress hypothesis than by the index argument. Evidence that developmental stress affects the January 2005] Perspectives in Ornithology 9 song system has so far been found on a gross ANDERSSON,M. 1994. . Princeton anatomical level only, but there is every reason University Press, Princeton, New Jersey. to believe that future studies will reveal cellular BAKER,M. C., AND M. A. CUNNINGHAM.1985. The and molecular consequences of stress that have biology of bird-song dialects. Behavioral an equally pronounced effect on behavior. and Brain Sciences 8:85-133. Thus, in the case of bird song, progress on BALLENTINE,B., J. HYMAN, AND S. NowICKI.2004. one of Tinbergen's four questions, that con- Vocal performance influences female re- cerning function, is made possible by work sponse to male bird song: An experimental on two others, those concerning development test. 15:163-168. and causation. In turn, a new hypothesis re- BAPTISTA, L. F., AND M. L. MORTON. 1988. garding function-the developmental stress Song learning in montane White-crowned hypothesis-has led to new studies probing the Sparrows: From whom and when? Animal development and causation of song, by study- Behaviour 36:1753-1764. ing the effects of early environmental stresses BAPTISTA,L. F., AND L. PETRINOVICH.1984. Social on neuroanatomy and on song learning. That interaction, sensitive phases and the song his four questions turn out each to have implica- template hypothesis in the White-crowned tions for the others presumably would not have Sparrow. Animal Behaviour 32:172-181. surprised Tinbergen. BAPTIsTA, L. F., AND L. PETRINOVICH. 1986. Song development in the White-crowned ACKNOWLEDGMENTS Sparrow: Social factors and sex differences. Animal Behaviour 34:1359-1371. We thank S. Peters for her help with all as- BECKER, P. H. 1982. The coding of species- pects of our research. The work was supported specific characteristics in bird sounds. by the National Science Foundation through Pages 213-252 in Acoustic grant IBN-0315377 to S.N. and grant IBN- in Birds (D. E. Kroodsma and E. H. Miller, 0315566 to W.A.S. Eds.). Academic Press, New York. BOTTJER,S. W., S. L. GLAESSNER,AND A. P.ARNOLD. LITERATURECITED 1985. Ontogeny of brain nuclei controlling song learning and behavior in Zebra Finches. AIREY,D. C., K. L. BUCHANAN,T. SZEKELY,C. K. Journal of 5:1556-1562. CATCHPOLE,AND T. J. DEVOOGD.2000. Song, BOTTJER,S. W., E. A. MIESNER,AND A. P. ARNOLD. sexual selection, and a song control nucleus 1984. Forebrain lesions disrupt develop- (HVC) in the brains of European Sedge ment but not maintenance of song in pas- Warblers. Journal of Neurobiology 44:1-6. serine birds. Science 224:901-903. AIREY,D. C., AND T. J. DEVOOGD.2000. Greater BRENOWITZ, E. A., B. NALLS, J. C. WINGFIELD, AND song complexity is associated with aug- D. E. KROODSMA.1991. Seasonal changes in mented song system in Zebra avian song nuclei without seasonal changes Finches. Neuroreport 11:2339-2344. in song repertoire. Journal of Neuroscience ALATALO, R. V., C. GLYNN, AND A. LUNDBERG. 11:1367-1374. 1990. Singing rate and female attraction in BUCHANAN, K. L., LEITNER, S., K. A. SPENCER, the Pied Flycatcher: An experiment. Animal A. R. GOLDSMITH, AND C. K. CATCHPOLE. Behaviour 39:601-603. 2004. Developmental stress selectively ALVAREZ-BUYALLA,A., C.-Y. LING,AND W. S. YU. affects the song control nucleus HCV in 1994. Contribution of neurons born dur- the Zebra . Proceedings of the Royal ing embryonic and adult life to the brain Society of London, Series B 271:2381-2386. of adult canaries: Regional specificity and BUCHANAN, K. L., K. A. SPENCER, A. R. GOLDSMITH, delayed birth of neurons in the song-control AND C. K. CATCHPOLE.2003. Song as an hon- nuclei. Journal of Comparative Neurology est signal of past developmental stress in 347:233-248. the European Starling (Sturnus vulgaris). ANDERSSON, M. 1986. Evolution of condition- Proceedings of the Royal Society of London, dependent sex ornaments and mating pref- Series B 270:1149-1156. erences: Sexual selection based on viability CATCHPOLE,C. K. 1980. Sexual selection and differences. Evolution 40:804-816. the evolution of complex songs among 10 Perspectivesin Ornithology [Auk, Vol. 122

European warblers of the genus Acrocephalus. FALLS, J. B. 1988. Does song deter territo- Behaviour 74:149-166. rial intrusion in White-throated Sparrows CATCHPOLE,C. K., J. DITTAMI, AND B. LEISLER. (Zonotrichia albicollis)? Canadian Journal of 1984. Differential responses to male song 66:206-211. repertoires in female songbirds implanted FISHER, R. A. 1930. The Genetical Theory of with oestradiol. Nature 312:563-564. . Clarendon Press, Oxford. CATCHPOLE,C. K., B. LEISLER, AND J. DITTAMI. GbRANSSON, G., G. HOGSTEDT, J. KARLSSON, 1986. Sexual differences in the responses of H. KALLANDER, AND S. ULFSTRAND. 1974. captive Great Reed Warblers (Acrocephalus Sangensroll for revirhallandet hos nakter- arundinaceus) to variation in song structure gal Luscinia luscinia-Nagra experiment and repertoire size. Ethology 73:69-77. med play-back-teknik. Var F'agelvarld 33: CATCHPOLE,C. K., AND P. J. B. SLATER.1995. Bird 201-209. Song: Biological Themes and Variations. GOTTLANDER, K. 1987. Variation in the song rate Cambridge University Press, Cambridge, of the male Pied Flycatcher Ficedula hypo- United . leuca: Causes and consequences. Animal CLAYTON,N. S., AND E. PR6VE. 1989. Song dis- Behaviour 35:1037-1043. crimination in female Zebra Finches and GRAFEN, A. 1990a. Biological signals as handi- Bengalese Finches. Animal Behaviour 38: caps. Journal of Theoretical Biology 144: 352-354. 517-546. COLLINS, S. A. 1999. Is female preference for GRAFEN, A. 1990b. Sexual selection unhandi- male repertoires due to sensory bias? capped by the Fisher process. Journal of Proceedings of the Royal Society of London, Theoretical Biology 144:473-516. Series B 266:2309-2314. GRAY, D. A., AND J. C. HAGELIN. 1996. Song DAvIEs, N. B., AND A. LUNDBERG. 1984. Food repertoires and sensory exploitation: distribution and a variable mating system in Reconsidering the case of the Common the Dunnock, Prunella modularis. Journal of Grackle. Animal Behaviour 52:795-800. Animal Ecology 53:895-912. HASSELQUIST, D. 1998. Polygyny in Great Reed DEVOOGD,T. J.,J. R. KREBS, S. D. HEALY,AND A. Warblers: A long-term study of factors PuRvis. 1993. Relations between song rep- contributing to male fitness. Ecology 79: ertoire size and the volume of brain nuclei 2376-2390. related to song: Comparative evolutionary HASSELQUIST, D., S. BENSCH, AND T. VON SCHANTZ. analyses amongst oscine birds. Proceedings 1996. Correlation between male song reper- of the Royal Society of London, Series B 254: toire, extra-pair paternity and offspring 75-82. survival in the Great Reed Warbler. Nature DRAGANOIU, T. I., L. NAGLE, AND M. KREUTZER. 381:229-232. 2002. Directional female preference for an HEYWOOD, J. S. 1989. Sexual selection by the exaggerated male trait in canary (Serinus handicap mechanism. Evolution 43:1387- canaria) song. Proceedings of the Royal 1397. Society of London, Series B 269:2525-2531. HINDE, R. A., AND E. STEEL. 1976. The effect of EENS, M., R. PINXTEN, AND R. F. VERHEYEN.1991. male song on an estrogen-dependent behav- Male song as a cue for mate choice in the ior pattern in the female canary (Serinus ca- European Starling. Behaviour 116:210-238. narius). Hormones and Behavior 7:293-304. EMLEN, S. T. 1972. An experimental analysis of HOELZER, G. A. 1989. The good parent process the parameters of bird song eliciting species of sexual selection. Animal Behaviour 38: recognition. Behaviour 41:130-171. 1067-1078. ENQUIST, M. 1985. Communication during HOESE, W. J., J. PODos, N. C. BOETTICHER,AND aggressive interactions with particular S. NOWICKI. 2000. Vocal tract function in reference to variation in choice of behaviour. birdsong production: Experimental ma- Animal Behaviour 33:1152-1161. nipulation of beak movements. Journal of ERIKSSON, D., AND L. WALLIN. 1986. Male bird Experimental Biology 203:1845-1855. song attracts females -A field experiment. HUXLEY, J. S. 1942. Evolution: The Modern Behavioral Ecology and 19: Synthesis. Allen and Unwin, London. 297-299. IWASA, Y., A. POMIANKOWSKI, AND S. NEE. 1991. January 2005] Perspectives in Ornithology 11

The evolution of costly mate preferences. MARLER, P., AND S. PETERS. 1988. Sensitive peri- II. The "handicap" principle. Evolution 45: ods for song acquisition from tape record- 1431-1442. ings and live tutors in the Swamp Sparrow, JOHNSON, L. S., AND W. A. SEARCY.1996. Female Melospiza georgiana. Ethology 77:76-84. attraction to male song in House Wrens MARLER, P., AND M. TAMURA. 1962. Song (Troglodytesaedon). Behaviour 133:357-366. "dialects" in three of White- JOHNSTONE, R. A. 1997. The evolution of ani- crowned Sparrows. Condor 64:368-377. mal signals. Pages 155-178 in Behavioural MAYNARD SMITH, J., AND D. HARPER. 1995. Ecology, 4th ed. (J. R. Krebs and N. B. Animal signals: Models and terminology. Davies, Eds.). Blackwell, Oxford. Journal of Theoretical Biology 177:305-311. KEMPENAERS, B., G. R. VERHEYEN, AND A. A. MAYNARD SMITH, J., AND D. HARPER. 2003. DHONDT. 1997. Extrapair paternity in the Animal Signals. Oxford University Press, Blue Tit (Parus caeruleus): Female choice, Oxford. male characteristics, and offspring quality. McDONALD, M. V. 1989. Function of song in Behavioral Ecology 8:481-492. Scott's Seaside Sparrow, Ammodramus KIRN, J. R., R. P. CLOWER,D. E. KROODSMA,AND maritimus peninsulae. Animal Behaviour 38: T. J. DEVOOGD. 1989. Song-related brain 468-485. regions in the Red-winged Blackbird are af- MCGREGOR, P. K. 1980. Song dialects in the Corn fected by sex and season but not repertoire Bunting (Emberiza calandra). Zeitschrift fur size. Journal of Neurobiology 20:139-163. Tierpsychologie 54:285-297. KONISHI, M. 1965. The role of auditory feed- MOONEY, R. 1999. Sensitive periods and circuit back in the control of vocalization in the for learned birdsong. Current Opinion in White-crowned Sparrow. Zeitschrift fur Neurobiology 9:121-127. Tierpsychologie 22:770-783. MOONEY, R., AND M. RAO. 1994. Waiting periods KONISHI, M., AND E. AKUTAGAWA. 1985. Neuronal versus early innervation: The development growth, atrophy and in a sexually of axonal connections in the Zebra Finch dimorphic song nucleus in the Zebra Finch song system. Journal of Neuroscience 14: brain. Nature 315:145-147. 6532-6543. KONISHI, M., S. T. EMLEN,R. E. RICKLEFS,AND J. C. MOUNTJOY, D. J., AND R. E. LEMON. 1991. Song as WINGFIELD.1989. Contributions of bird stud- an attractant for male and female European ies to biology. Science 246:465-472. Starlings, and the influence of song com- KREBS,J. R. 1977. Song and territory in the Great plexity on their response. Behavioral Tit. Pages 47-62 in Ecology and Sociobiology 28:97-100. (B. Stonehouse and C. M. Perrins, Eds.). MOUNTJOY, D. J., AND R. E. LEMON. 1996. Female MacMillan and Company, London. choice for complex song in the European KROODSMA,D. E. 1976. Reproductive develop- Starling: A field experiment. Behavioral ment in a female songbird: Differential Ecology and Sociobiology 38:65-71. stimulation by quality of male song. Science NELSON, D. A. 1998. External validity and exper- 192:574-575. imental design: The sensitive phase for song LACOMBE,D., D. M. BIRD, AND K. A. HIBBARD. learning. Animal Behaviour 56:487-491. 1994. Influence of reduced food availability NORDEEN, K. W., P. MARLER, AND E. J. NORDEEN. on growth of captive American Kestrels. 1989. Addition of song-related neurons in Canadian Journal of Zoology 72:2084-2089. Swamp Sparrows coincides with memori- MARLER, P. 1970. A comparative approach to zation, not production, of learned songs. : Song development in White- Journal of Neurobiology 20:651-661. crowned Sparrows. Journal of Comparative NORDEEN, E. J., AND K. W. NORDEEN. 1988. Sex and Physiological Psychology 71:1-25. and regional differences in the incorporation MARLER,P., AND S. PETERS.1977. Selective vocal of neurons born during song learning in learning in a sparrow. Science 198:519-521. Zebra Finches. Journal of Neuroscience 8: MARLER,P., AND S. PETERS. 1987. A sensitive peri- 2869-2874. od for song acquisition in the Song Sparrow, NOTTEBOHM, F. 1972. The origins of vocal learn- Melsopiza melodia: A case of age-limited ing. American Naturalist 106:116-140. learning. Ethology 76:89-100. NOTTEBOHM, F., S. KASPARIAN, AND C. PANDAZIS. 12 Perspectivesin Ornithology [Auk, Vol. 122

1981. Brain space for a learned task. Brain PEEK, F. W. 1972. An experimental study of Research213:99-109. the territorial function of vocal and visual NOTTEBOHM,F., M. E. NOTTEBOHM,AND L. display in the male Red-winged Blackbird .1986. Developmental and seasonal (Agelaius phoeniceus). Animal Behaviour 20: changes in canary song and their relation 112-118. to changes in the anatomy of song-control PETRINOVICH, L., AND L. F. BAPTISTA. 1987. nuclei. Behavioral and Neural Biology 46: Song development in the White-crowned 445-471. Sparrow: Modification of learned song. NOTTEBOHM,F., T. M. STOKES,AND C. M. Animal Behaviour 35:961-974. LEONARD.1976. Central control of song PODOS,J. 1997. A performance constraint on the in the canary, Serinus canarius. Journal of evolution of trilled vocalizations in a song- Comparative Neurology 165:457-486. bird (Passeriformes: Emberizidae). NOWICKI,S. 1987. Vocal tract resonances in os- Evolution 51:537-551. cine bird sound production: Evidence from PODOS,J. 2001. Correlated evolution of morphol- birdsongs in a helium atmosphere. Nature ogy and vocal signals in Darwin's finches. 325:53-55. Nature 409:185-188. NoWICKI, S., D. HASSELQUIST,S. BENSCH, AND PODOS,J., J.K. SHERER,S. PETERS,AND S. NOWICKI. S. PETERS. 2000. Nestling growth and song 1995. Ontogeny of vocal tract movements repertoire size in Great Reed Warblers: during song production in Song Sparrows. Evidence for song learning as an indicator Animal Behaviour 50:1287-1296. mechanism in mate choice. Proceedings of PODOS,J., J. A. SOUTHALL, AND M. R. Rossi- the Royal Society of London, Series B 267: SANTOS. 2004. Vocal mechanics in Darwin's 2419-2424. finches: Correlation of beak gape and song NOWICKI,S., S. PETERS,AND J. PODOS.1998a. frequency. Journal of Experimental Biology Song learning, early nutrition and sexual 207:607-619. selection in songbirds. American Zoologist POMIANKOWSKI, A. 1987. Sexual selection: 38:179-190. The handicap mechanism does work- NoWICKI, S., AND W. A. SEARCY.2004. Song Sometimes. Proceedings of the Royal Society function and the evolution of female pref- of London, Series B 231:123-145. erences: Why birds sing and why brains PUSEY, A., AND M. WOLF. 1996. Inbreeding avoid- matter. Pages 704-723 in The Behavioral ance in animals. Trends in Ecology and Neurobiology of Bird Song (H. P. Ziegler Evolution 11:201-206. and P. Marler, Eds.). New York Academy of REID, J. M., P. ARCESE, A. L. E. V. CASSIDY,S. M. Sciences, New York. HIEBERT, J. N. M. SMITH, P. K. STODDARD, NowICKI, S., W. A. SEARCY, AND M. HUGHES. A. B. MARR, AND L. F. KELLER. 2004. Song 1998b. The territory defense function of repertoire size predicts initial mating suc- song in Song Sparrows: A test with the cess in male Song Sparrows, Melospiza melo- speaker occupation design. Behaviour 135: dia. Animal Behaviour 68:1055-1063. 615-628. RICHNER, H., P. SCHNEITER, AND H. STIRNIMANN. NowICKI, S., W. A. SEARCY, AND S. PETERS.2002a. 1989. Life-history consequences of growth Brain development, song learning and mate rate depression: An experimental study on choice in birds: A review and experimental Carrion Crows (Corvus corone corone L.). test of the "nutritional stress hypothesis." Functional Ecology 3:617-624. Journal of Comparative A 188: RYAN, M. J. 1998. Sexual selection, receiver bi- 1003-1014. ases, and the evolution of sex differences. NowICKI, S., W. A. SEARCY, AND S. PETERS. 2002b. Science 281:1999-2003. Quality of song learning affects female RYAN, M. J., AND A. S. RAND. 1993. Sexual selection response to male bird song. Proceedings of and signal evolution: The ghost of biases the Royal Society of London, Series B 269: past. Philosophical Transactions of the Royal 1949-1954. Society of London, Series B 340:187-195. OBERWEGER,K., AND F. GOLLER.2001. The meta- SCHLUTER, D., AND J. N. M. SMITH. 1986. Natural bolic cost of birdsong production. Journal of selection on beak and body size in the Song Experimental Biology 204:3379-3388. Sparrow. Evolution 40:221-231. January2005] Perspectivesin Ornithology 13

SEARCY,W. A. 1979. Sexual selection and body 1990. Selective impairment of song learning size in male Red-winged Blackbirds. following lesions of a forebrain nucleus in Evolution 33:649-661. the juvenile Zebra Finch. Behavioral and SEARCY, W. A. 1984. Song repertoire size and Neural Biology 53:51-63. female preferences in Song Sparrows. SPENCER, K. A., K. L. BUCHANAN, A. R. Behavioral Ecology and Sociobiology 14: GOLDSMITH, AND C. K. CATCHPOLE. 2003. 281-286. Song as an honest signal of developmental SEARCY,W. A. 1992a. Measuring responses of stress in the Zebra Finch (Taeniopygia gut- female birds to male song. Pages 175-189 tata). Hormones and Behavior 44:132-139. in Playback and Studies of Animal SPENCER, K.A., K.L. BUCHANAN, A. R. GOLDSMITH, Communication. (P. K. McGregor, Ed.). AND C. K. CATCHPOLE. 2004. Developmental Plenum Press, New York. stress, social rank and song complexity in SEARCY,W. A. 1992b. Song repertoires and mate the European Starling (Sturnus vulgaris). choice in birds. American Zoologist 32: Proceedings of the Royal Society of London, 71-80. Series B 271:S121-S123. SEARCY,W. A., AND M. ANDERSSON. 1986. Sexual SZEKELY, T., C. K. CATCHPOLE, A. DEVOOGD, selection and the evolution of song. Annual Z. MARCHL, AND T. J. DEVOOGD. 1996. Review of Ecology and Systematics 17: Evolutionary changes in a song control area 507-533. of the brain (HVC) are associated with evo- SEARCY,W. A., AND P. MARLER. 1981. A test for lutionary changes in song repertoire among responsiveness to song structure and pro- European warblers (Sylviidae). Proceedings gramming in female sparrows. Science 213: of the Royal Society of London, Series B 263: 926-928. 607-610. SEARCY,W. A., AND S. NOWICKI. 2000. Male-male THORPE, W. H. 1958. The learning of song pat- competition and female choice in the evo- terns by birds, with especial reference to the lution of vocal signaling. Pages 301-315 song of the chaffinch, Fringilla coelebs. Ibis in Animal Signals: Signalling and Signal 100:535-570. Design in Animal Communication (Y. TINBERGEN, N. 1951. The Study of . Espmark, T. Amundsen, and G. Rosenqvist, Oxford University Press, Oxford. Eds.). Tapir Academic Press, Trondheim. TINBERGEN, N. 1963. On aims and methods of SEARCY, W. A., AND S. NowICKI. 2005. The ethology. Zeitschrift fur Tierpsychologie 20: Evolution of Animal Communication: 410-433. Reliability and Deception in Signaling VALLET, E., I. BEME, AND M. KREUTZER. 1998.Two- Systems. Princeton University Press, note syllables in canary songs elicit high Princeton, New Jersey. In press. levels of sexual display. Animal Behaviour SEARCY, W. A., S. NOWICKI, M. HUGHES, AND S. 55:291-297. PETERS. 2002. Geographic song discrimina- VALLET, E., AND M. KREUTZER. 1995. Female tion in relation to dispersal distances in Song canaries are sexually responsive to spe- Sparrows. American Naturalist 159:221-230. cial song phrases. Animal Behaviour 49: SEARCY, W. A., S. PETERS, AND S. NowICKI.2004. 1603-1610. Effects of early nutrition on growth rate and WARD, S., H. LAMPE, AND P. J. B. SLATER. 2004. adult size in Song Sparrows Melospiza melo- Singing is not energetically demanding dia. Journal of Avian Biology 35:269-279. for Pied Flycatchers, Ficedula hypoleuca. SMITH, D. G. 1979. Male singing ability and ter- Behavioral Ecology 15:477-484. ritory integrity in Red-winged Blackbirds WARD, S., J. R. SPEAKMAN, AND P. J. B. SLATER. (Agelaius phoeniceus). Behaviour 68:193-206. 2003. The energy cost of song in the canary, SMITH, G. T., E. A. BRENOWITZ, M. D. BEECHER, Serinus canaria. Animal Behaviour 66: AND J. C. WINGFIELD. 1997. Seasonal changes 893-902. in testosterone, neural attributes of song WASSERMAN, F. E., AND J. A. CIGLIANO. 1991. control nuclei, and song structure in wild Song output and stimulation of the female songbirds. Journal of Neuroscience 17: in White-throated Sparrows. Behavioral 6001-6010. Ecology and Sociobiology 29:55-59. SOHRABJI, F., E. J. NORDEEN, AND K. W. NORDEEN. WEATHERHEAD, P. J., AND P. T. BOAG. 1995. Pair 14 Perspectivesin Ornithology [Auk, Vol. 122

and extra-pair mating success relative to in the European Starling. Behaviour 120: male quality in Red-winged Blackbirds. 262-285. Behavioral Ecology and Sociobiology 37: YASUKAWA,K. 1981. Song and territory defense in 81-91. the Red-winged Blackbird. Auk 98:185-187. WESTNEAT,M. W., J. H. LONG, W. HOESE,AND ZAHAVI, A. 1975. Mate selection-A selection for S. NOWICKI.1993. Kinematics of birdsong: a handicap. Journal of Theoretical Biology Functional correlation of cranial movements 53:205-214. and acoustic features in sparrows. Journal of ZAHAVI,A. 1977. The cost of honesty (further Experimental Biology 182:147-171. remarks on the handicap principle). Journal WRIGHT, J., AND I. CUTHILL. 1992. Monogamy of Theoretical Biology 67:603-605.