THE INFLUENCE OF THE CALIFORNIA MARINE LAYER ON BILL SIZE IN A GENERALIST SONGBIRD

The hypothesis is tested that birds in hotter and drier environments may have larger bills to increase the surface area for heat dissipation. California provides a climatic gradient to test the influence of climate on bill size. Much of California experiences dry warm/hot summers and coastal areas experience cooler summers than interior localities. Based on measurements from 1488 museum skins, song sparrows showed increasing body‐size‐corrected bill surface area from the coast to the interior and declining in the far eastern desert. As predicted by Newton's convective heat transfer equation, relative bill size increased monotonically with temperature, and then decreased where average high temperatures exceed body temperature. Of the variables considered, distance from coast, average high summer temperature, and potential evapotranspiration showed a strong quadratic association with bill size and rainfall had a weaker negative relationship. Song sparrows on larger, warmer islands also had larger bills. A subsample of radiographed specimens showed that skeletal bill size is also correlated with temperature, demonstrating that bill size differences are not a result of variation in growth and wear of keratin. Combined with recent thermographic studies of heat loss in song sparrow bills, these results support the hypothesis that bill size in California song sparrows is selected for heat dissipation.     

The 'island rule' in birds: medium body size and its ecological explanation

Do birds show a different pattern of insular evolution from mammals? Mammals follow the ''island rule'', with large-bodied species getting smaller on islands and small-bodied species getting bigger. By contrast, the traditional view on birds is that they follow no general island rule for body size, but that there is an insular trend for large bills. Insular shifts in feeding ecology are, therefore, widely assumed to be the primary cause of divergence in island birds. We use a comparative approach to test these ideas. Contrary to the traditional view, we find no evidence for increased bill size in insular populations. Instead, changes in both bill size and body size obey the ''island rule''. The differences between our results and the traditional view arise because previous analyses were based largely on passerines. We also investigate some ecological factors that are thought to influence island evolution. As predicted by the traditional view, shifts in bill size are associated with feeding ecology. By contrast, shifts in body size are associated with the potential for intraspecific competition and thermal ecology. All these results remain qualitatively unchanged when we use different methods to score the ecological factors and restrict our analyses to taxa showing pronounced morphological divergence. Because of strong covariation between ecological factors, however, we cannot estimate the relative importance of each ecological factor. Overall, our results show that the island rule is valid for both body size and bill length in birds and that, in addition to feeding ecology, insular shifts in the level of intraspecific competition and the abiotic environment also have a role.     

Innate differences in singing behaviour of sparrows reared in isolation from adult conspecific song

Innate differences in the singing behaviour of male swamp (Melospiza georgiana) and song (M. melodia) sparrows were identified by rearing males from the egg in the laboratory under identical conditions, in complete isolation from adult conspecific song. Isolation-reared males of both species displayed several abnormal song features, including reduced numbers of notes per song, longer durations of notes and inter-note intervals, and fewer notes per syllable. Despite these and other abnormalities, many species differences emerged that matched differences in the natural singing behaviour of the two species. These included differences in song repertoire size, song duration and degrees of segmentation, numbers of notes per song, durations of notes and inter-note intervals, and several measures reflecting the organization of songs into note complexes, syllables and trills. Although learning can influence all levels of organization of the motor patterns of song in swamp and song sparrows, its contribution to the achievement of normal song behaviour appears to be most crucial at the level of the fine structure of the notes and syllables from which the songs are constructed.     

A biogeographic pattern in sparrow bill morphology: parallel adaptation to tidal marshes

The study of ecological convergence, the evolution of similar traits on multiple occasions in response to similar conditions, is a powerful method for developing and testing adaptive hypotheses. However, despite the great attention paid to geographic variation and the foraging ecology of birds, surprisingly few cases of convergent or parallel feeding adaptations have been adequately documented. In this study, we document a biogeographic pattern of parallel bill morphology across 10 sparrow taxa endemic to tidal marshes. All North American tidal marsh sparrows display parallel differentiation from close relatives in other habitats, suggesting that selection on bill morphology is strong. Relative to their body mass, tidal marsh sparrows have longer, thinner bills than their non-tidal marsh counterparts, which is likely an adaptation for consuming more invertebrates and fewer seeds, as well as for probing in sediment crevices to capture prey. Published data on tidal marsh food resources and diet of the relevant taxa support this hypothesis. This morphological differentiation is most pronounced between sister taxa with the greatest estimated divergence times, but is found even in taxa that show little or no structure in molecular genetic markers. We, therefore, speculate that tidal marsh ecosystems are likely settings for ecological speciation.     

A Tradeoff Between Performance and Accuracy in Bird Song Learning

Some of nature’s most complex behaviors, such as human speech and oscine bird song, are acquired through imitative learning. Accurate imitative learning tends to preserve patterns of behavior across generations, thus limiting the scope of cultural evolution. Less well studied are the routes by which cultural novelties arise during development, beyond simple copy error. In this study we assess, in a species of songbird, the relationship in song learning between two potentially conflicting learning goals: accuracy in copying and maximization of vocal performance. In our study species, the swamp sparrow (Melospiza georgiana), vocal performance can be defined for a given song type and frequency range by the rate of note repetition (‘trill rate’), with faster trills being more difficult to sing. We trained young swamp sparrows with song models with experimentally modified trill rates and characterized both the accuracy and performance levels of copies. Our main finding is that birds elevated the trill rates of low‐performance models, but at the expense of imitative accuracy. By contrast, birds reproduced normal and high‐performance models with typically high accuracy in structure and timing. Developmental mechanisms that enable songbirds to balance imitative accuracy and vocal performance are likely favored by sexual selection and may help explain some current patterns of variation in birdsong. Such mechanisms may also explain how behaviors that are learned by imitation can nevertheless respond to selection for high‐performance levels in their expression.     

Common Garden Experiment Reveals Genetic Control of Phenotypic Divergence between Swamp Sparrow Subspecies That Lack Divergence in Neutral Genotypes

Background

Adaptive divergence between populations in the face of strong selection on key traits can lead to morphological divergence between populations without concomitant divergence in neutral DNA. Thus, the practice of identifying genetically distinct populations based on divergence in neutral DNA may lead to a taxonomy that ignores evolutionarily important, rapidly evolving, locally-adapted populations. Providing evidence for a genetic basis of morphological divergence between rapidly evolving populations that lack divergence in selectively neutral DNA will not only inform conservation efforts but also provide insight into the mechanisms of the early processes of speciation. The coastal plain swamp sparrow, a recent colonist of tidal marsh habitat, differs from conspecific populations in a variety of phenotypic traits yet remains undifferentiated in neutral DNA.

Methods and Principal Findings

Here we use an experimental approach to demonstrate that phenotypic divergence between ecologically separated populations of swamp sparrows is the result of local adaptation despite the lack of divergence in neutral DNA. We find that morphological (bill size and plumage coloration) and life history (reproductive effort) differences observed between wild populations were maintained in laboratory raised individuals suggesting genetic divergence of fitness related traits.

Conclusions and Significance

Our results support the hypothesis that phenotypic divergence in swamps sparrows is the result of genetic differentiation, and demonstrate that adaptive traits have evolved more rapidly than neutral DNA in these ecologically divergent populations that may be in the early stages of speciation. Thus, identifying evolutionarily important populations based on divergence in selectively neutral DNA could miss an important level of biodiversity and mislead conservation efforts.     

Heat Loss May Explain Bill Size Differences between Birds Occupying Different Habitats

Background

Research on variation in bill morphology has focused on the role of diet. Bills have other functions, however, including a role in heat and water balance. The role of the bill in heat loss may be particularly important in birds where water is limiting. Song sparrows localized in coastal dunes and salt marsh edge (Melospiza melodia atlantica) are similar in size to, but have bills with a 17% greater surface area than, those that live in mesic habitats (M. m. melodia), a pattern shared with other coastal sparrows. We tested the hypotheses that sparrows can use their bills to dissipate “dry” heat, and that heat loss from the bill is higher in M. m. atlantica than M. m. melodia, which would indicate a role of heat loss and water conservation in selection for bill size.

Methodology/Principal Findings

Bill, tarsus, and body surface temperatures were measured using thermal imaging of sparrows exposed to temperatures from 15–37°C and combined with surface area and physical modeling to estimate the contribution of each body part to total heat loss. Song sparrow bills averaged 5–10°C hotter than ambient. The bill of M. m atlantica dissipated up to 33% more heat and 38% greater proportion of total heat than that of M. m. melodia. This could potentially reduce water loss requirements by approximately 7.7%.

Conclusions/Significance

This >30% higher heat loss in the bill of M. m. atlantica is independent of evaporative water loss and thus could play an important role in the water balance of sparrows occupying the hot and exposed dune/salt marsh environments during the summer. Heat loss capacity and water conservation could play an important role in the selection for bill size differences between bird populations and should be considered along with trophic adaptations when studying variation in bill size.     

Vocal performance influences female response to male bird song: an experimental test

Female songbirds are thought to assess males based on aspectsof song, such as repertoire size or amount of singing, thatcould potentially provide information about male quality. Arelatively unexplored aspect of song that also might serve asan assessment signal is a male's ability to perform physicallychallenging songs. Trilled songs, such as those produced byswamp sparrows (Melospiza georgiana), present males with a performancechallenge because trills require rapid and precise coordinationof vocal tract movements, resulting in a trade-off between trillrate and frequency bandwidth. This trade-off defines a constrainton song production observed as a triangular distribution inacoustic space of trill rate by frequency bandwidth, with anupper boundary that represents a performance limit. Given thisbackground on song production constraints, we are able to identifya priori which songs are performed with a higher degree of proficiencyand, thus, which songs should be more attractive to females.We determined the performance limit for a population of swampsparrows and measured how well individual males performed songsrelative to this limit ("vocal performance"). We then comparedfemale solicitation responses to high-performance versus low-performanceversions of the same song type produced by different males.Females displayed significantly more to high-performance songsthan to low-performance songs, supporting the hypothesis thatfemales use vocal performance to assess males.     

Addition of song-related neurons in swamp sparrows coincides with memorization, not production, of learned songs

During song learning in birds, neurons are added to some song nuclei and lost from others. Previous studies have been unable to distinguish whether these neural changes are uniquely associated with memorizing a song model (sensory acquisition) or vocal practice (sensorimotor learning). In this study we measured changes in neuron number within song nuclei of swamp sparrows, a species in which the two phases of song learning are nonoverlapping. Male swamp sparrows were collected as hatchlings and tape-tutored from approximately 22 to 62 days of age. Swamp sparrows memorize about 60% of their song material during this period, but do not begin practicing this learned material until approximately 275 days of age. Birds were sacrificed at 23, 41, 61, 71, 274, or 340 days of age. During sensory acquisition, neuron number increased drastically in both the caudal nucleus of the ventral hyperstriatum (HVc) and Area X. The period of sensorimotor learning was not associated with any further changes in neuron number within these regions. We were unable to detect any significant changes in neuron number within the magnocellular nucleus of the neostriatum or the robust nucleus of the archistriatum during either stage of song learning. These results raise the possibility that ongoing addition of HVc and Area X neurons may encourage, and thereby temporally restrict, song acquisition.     

Song characteristics track bill morphology along a gradient of urbanization in house finches (<Emphasis Type="Italic">Haemorhous mexicanus</Emphasis>)

Introduction

Urbanization can considerably impact animal ecology, evolution, and behavior. Among the new conditions that animals experience in cities is anthropogenic noise, which can limit the sound space available for animals to communicate using acoustic signals. Some urban bird species increase their song frequencies so that they can be heard above low-frequency background city noise. However, the ability to make such song modifications may be constrained by several morphological factors, including bill gape, size, and shape, thereby limiting the degree to which certain species can vocally adapt to urban settings. We examined the relationship between song characteristics and bill morphology in a species (the house finch, Haemorhous mexicanus) where both vocal performance and bill size are known to differ between city and rural animals.

Results

We found that bills were longer and narrower in more disturbed, urban areas. We observed an increase in minimum song frequency of urban birds, and we also found that the upper frequency limit of songs decreased in direct relation to bill morphology.

Conclusions

These findings are consistent with the hypothesis that birds with longer beaks and therefore longer vocal tracts sing songs with lower maximum frequencies because longer tubes have lower-frequency resonances. Thus, for the first time, we reveal dual constraints (one biotic, one abiotic) on the song frequency range of urban animals. Urban foraging pressures may additionally interact with the acoustic environment to shape bill traits and vocal performance.

     

The effects of translocation-induced isolation and fragmentation on the cultural evolution of bird song

Understanding the divergence of behavioural signals in isolated populations is critical to knowing how certain barriers to gene flow can develop. For many bird species, songs are essential for conspecific recognition and mate choice. Measuring the rate of song divergence in natural populations is difficult, but translocations of endangered birds to isolated islands for conservation purposes can yield insights, as the age and source of founder populations are completely known. We found significant and rapid evolution in the structure and diversity of bird song in North Island saddlebacks, Philesturnus rufusater, in New Zealand, with two distinct lineages evolving in < 50 years. The strong environmental filters of serial translocations resulted in cultural bottlenecks that generated drift and reduced song variability within islands. This rapid divergence coupled with loss of song diversity has important implications for the behavioural evolution of this species, demonstrating previously unrecognised biological consequences of conservation management.     

The effects of contemporary processes in maintaining the genetic structure of western song sparrows (Melospiza melodia)

Historic events and contemporary processes work in concert to create and maintain geographically partitioned variation and are instrumental in the generation of biodiversity. We sought to gain a better understanding of how contemporary processes such as movement and isolation influence the genetic structure of widely distributed vagile species such as birds. Song sparrows (Melospiza melodia) in western North America provide a natural system for examining the genetics of populations that have different patterns of geographic isolation and migratory behavior. We examined the population genetics of 576 song sparrows from 23 populations using seven microsatellite loci to assess genetic differentiation among populations and to estimate the effects of drift and immigration (gene flow) on each population. Sedentary, isolated populations were characterized by low levels of immigration and high levels of genetic drift, whereas those populations less isolated displayed signals of high gene flow and little differentiation from other populations. Contemporary dispersal rates from migratory populations, estimated by assignment test, were higher and occurred over larger distances than dispersal from sedentary populations but were also probably too low to counter the effects of drift in most populations. We suggest that geographic isolation and limited gene flow facilitated by migratory behavior are responsible for maintaining observed levels of differentiation among Pacific coastal song sparrow populations.     

Species song discrimination in choice experiments with territorial male swamp and song sparrows

Playbacks of synthetic and normal songs were used to determine what song parameters are important to species song recognition by territorial male swamp sparrows (Melospiza georgiana) and song sparrows (Melospiza melodia). Syllable morphology influences the discrimination of conspecific song from song sparrow song in adult swamp sparrows, but temporal pattern does not; this result duplicates that found in studies of song learning of the young in this species. Species song recognition is influenced by both syllable morphology and temporal pattern in adult song sparrows, in contrast to the situation in young sparrows, which seem not to distinguish their own species' song from that of swamp sparrows on either cue.     

Evolution on a local scale: developmental, functional, and genetic bases of divergence in bill form and associated changes in song structure between adjacent habitats

Divergent selection on traits involved in both local adaptation and the production of mating signals can strongly facilitate population differentiation. Because of its links to foraging morphologies and cultural inheritance song of birds can contribute particularly strongly to maintenance of local adaptations. In two adjacent habitats--native Sonoran desert and urban areas--house finches (Carpodacus mexicanus) forage on seeds that are highly distinct in size and shell hardness and require different bite forces and bill morphologies. Here, we first document strong and habitat-specific natural selection on bill traits linked to bite force and find adaptive modifications of bite force and bill morphology and associated divergence in courtship song between the two habitats. Second, we investigate the developmental basis of this divergence and find that early ontogenetic tissue transformation in bill, but not skeletal traits, is accelerated in the urban population and that the mandibular primordia of the large-beaked urban finches express bone morphogenetic proteins (BMP) earlier and at higher level than those of the desert finches. Further, we show that despite being geographically adjacent, urban and desert populations are nevertheless genetically distinct corroborating findings of early developmental divergence between them. Taken together, these results suggest that divergent selection on function and development of traits involved in production of mating signals, in combination with localized learning of such signals, can be very effective at maintaining local adaptations, even at small spatial scales and in highly mobile animals.     

Hearing in the swamp sparrow,Melospiza georgiana,and the song sparrow,Melospiza melodia

Operant conditioning techniques and a psychophysical tracking procedure were used to measure thresholds for pure tones in two congeneric species of sparrows: swamp sparrows and song sparrows. Thresholds were measured both in quiet conditions and in the presence of white noise. The two species were similar in their gross pattern of auditory sensitivity with most sensitive thresholds in the frequency region of 1·0–8·0 kHz and poor hearing above and below this range. However, the best sensitivity occurred at 2 kHz for the song sparrows and at 4 kHz for the swamp sparrows. This pattern was also observed in song spectra of the two species. The songs of song sparrows had more power in lower frequencies than the songs of swamp sparrows. Masked auditory thresholds for both species were very similar, showing a generally increasing signal-to-noise ratio with increasing frequency. The similarity between swamp and song sparrows in these measures of basic auditory sensitivity suggests that the primary mechanisms underlying selective vocal learning in these sparrows probably reside at higher levels than the peripheral auditory sensitivities.     

Causes of reduced clutch size in a tidal marsh endemic

We tested three hypotheses of clutch size variation in two subspecies of the swamp sparrow (Melospiza georgiana georgiana and M. g. nigrescens). Swamp sparrows follow the pattern of other estuarine endemics, where clutch size is smaller among tidal salt marsh populations (M. g. nigrescens) than their closest inland relatives (M. g. georgiana). Our results support predation risk and temperature, but not adult survival, as explanations of this pattern in swamp sparrows. Coastal nests were twice as likely to fail as inland nests, and parental activity around the nest site was positively related to clutch size at both sites. When brood size was controlled for, coastal adults visited nests less often and females vocalized less frequently during visits than inland birds, which may decrease nest detectability to predators. Coastal parents waited longer than inland birds to feed offspring in the presence of a model nest predator, but there was no difference in their response to models of predators of adults, as would be expected if coastal birds possessed increased longevity. Additionally, coastal females laid more eggs than inland females over a single season, following a within-season bet-hedging strategy rather than reducing within-season investment. Coastal territories experienced ambient air temperatures above the physiological zero of egg development more often, and higher temperatures during laying correlated with smaller clutches and increased egg inviability among coastal birds. Similar effects were not seen among inland nests, where laying temperatures were generally below physiological zero. Both subspecies showed an increase in hatching asynchrony and a decrease in apparent incubation length under high temperatures. Coastal individuals, however, showed less hatching asynchrony overall despite higher temperatures. Both air temperatures during laying and predation risk could potentially explain reduced clutch size in not only coastal plain swamp sparrows, but also other tidal marsh endemics.     

The role of the pineal gland in the photoperiodic control of bird song frequency and repertoire in the house sparrow, Passer domesticus

Temperate zone birds are highly seasonal in many aspects of their physiology. In mammals, but not in birds, the pineal gland is an important component regulating seasonal patterns of primary gonadal functions. Pineal melatonin in birds instead affects seasonal changes in brain song control structures, suggesting the pineal gland regulates seasonal song behavior. The present study tests the hypothesis that the pineal gland transduces photoperiodic information to the control of seasonal song behavior to synchronize this important behavior to the appropriate phenology. House sparrows, Passer domesticus, expressed a rich array of vocalizations ranging from calls to multisyllabic songs and motifs of songs that varied under a regimen of different photoperiodic conditions that were simulated at different times of year. Control (SHAM) birds exhibited increases in song behavior when they were experimentally transferred from short days, simulating winter, to equinoctial and long days, simulating summer, and decreased vocalization when they were transferred back to short days. When maintained in long days for longer periods, the birds became reproductively photorefractory as measured by the yellowing of the birds' bills; however, song behavior persisted in the SHAM birds, suggesting a dissociation of reproduction from the song functions. Pinealectomized (PINX) birds expressed larger, more rapid increases in daily vocal rate and song repertoire size than did the SHAM birds during the long summer days. These increases gradually declined upon the extension of the long days and did not respond to the transfer to short days as was observed in the SHAM birds, suggesting that the pineal gland conveys photoperiodic information to the vocal control system, which in turn regulates song behavior.     

Species song discrimination in adult female song and swamp sparrows

Six female song sparrows (Melospiza melodia) and six female swamp sparrows (Melospiza georgiana) were treated with oestradiol, and their response to song measured by frequency and intensity of copulation-solicitation display. Test stimuli were synthetic songs composed of either song sparrow or swamp sparrow syllables assembled in either song-sparrow-like or swamp-sparrow-like temporal patterns. Female song sparrows responded preferentially to songs containing their own species' syllables and to songs containing their own species' temporal patterns. Swamp sparrows were also sensitive to both syllable type and temporal, pattern, in contrast to male swamp sparrows, which show no preference for swamp sparrow temporal patterns.     

High summer temperature explains bill size variation in salt marsh sparrows

Physiological factors are rarely proposed to account for variation in the morphology of feeding structures. Recently, bird bills have been demonstrated to be important convective and radiant heat sinks. Larger bills have greater surface area than smaller bills and could serve as more effective thermoregulatory organs under hot conditions. The heat radiating function of bills should be more important in open habitats with little shade and stronger convective winds. Furthermore, as a means of dumping heat without increasing water loss through evaporation, bills might play a particularly important thermoregulatory role in heat loss in windy habitat where fresh water is limited. North American salt marshes provide a latitudinal gradient of relatively homogeneous habitat that is windy, open, and fresh‐water limited. To examine the potential role of thermoregulation in determining bill size variation among ten species or subspecies of tidal marsh sparrows, we plotted bill size against maximum summer and minimum winter temperatures. Bill surface areas increases with summer temperature, which explained 82–89% of the variance (depending upon sex) when we controlled for genus membership. Latitude alone predicted bill surface area much more poorly than summer temperature, and winter temperatures explained < 10% of the variance in winter bill size. Tidal marsh sparrow bill morphology may, to a large degree, reflect the role of the bill in expelling excess body heat in these unbuffered, fresh‐water‐limited environments. This new example of Allen's rule reaffirms the importance of physiological constraints on the evolution of vertebrate morphologies, even in bird bills, which have conventionally been considered as products of adaptation to foraging niche.     

Morphological adaptation to coastal marshes in spite of limited genetic structure in the Neotropical passerine Spartonoica maluroides (Aves: Furnariidae)

Tidal marshes present profound adaptive challenges to terrestrial vertebrates. For example, North American sparrows have relatively longer and thinner bills and darker dorsal plumage in coastal saltmarshes than in interior marshes. Bay‐capped wren‐spinetail (Furnariidae; Spartonoica maluroides) show a strong association with South American saltmarshes. We hypothesized that bay‐capped wren‐spinetail have similar morphological adaptations to North American sparrows to the saltmarsh environment, which would be indicative of the generality of selection on these traits in the coastal saltmarsh ecosystem. We captured individuals of S. maluroides from coastal saltmarshes and interior marshes. Populations were compared based on morphology and molecular markers. We found significant phenotypic differences in bill shape and plumage coloration (melanism) between S. maluroides populations from coastal and inland marshes. The low levels of genetic variation, weak geographical structure and shallow divergences, based on mitochondrial DNA and microsatellite data, suggest that coastal populations had a recent demographic expansion. Our results are consistent with the pattern of morphological divergence found between North American Emberizids. The possibility of convergent evolutionary adaptations between saltmarsh North American Emberizids and South American Furnariids suggests that there are strong selective pressures associated with saltmarsh environments on the beak, leading to adaptations for food acquisition, and on plumage coloration for better camouflage for predator avoidance (melanism). © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 78–91.