Variable energetic responses to clutch size manipulations in white-throated dippers Cinclus cinclus

We used the doubly-labelled water technique to measure daily energy expenditure (DEE) of a free-living uniparental incubator, the white-throated dipper Cinclus cinclus , in Scotland. DEE was 205±8 (s.e.m.) kJ d⁻¹ for 17 females incubating their natural clutch sizes, equivalent to 3.2±0.1×basal metabolic rate (BMR). To investigate the influence of clutch size on the energy budget, we measured the DEE of 14 females with clutches increased or reduced by a single egg. Birds with reduced clutch sizes had an energy expenditure with a mean and variance that did not differ from those of birds with unmanipulated clutches. Enlarging the clutch led to an increase in energy expenditure to over 4×BMR for some individuals but not for others, resulting in greater variance in energy expenditure for birds with enlarged clutches. Individual variation in energy expenditure could not be fully explained by environmental conditions, by patterns of behaviour or clutch size. Incubating females received a maximum of only 4 kJ d⁻¹ (2% of DEE) from provisioning by the male, and mobilised up to 6 kJ d⁻¹ (3% of DEE) from reserves. Females spent 2.9±0.2 h (n=20) away from the nest each day, so a foraging rate of 95 kJ h⁻¹ was required during incubation recesses to balance DEE. This 'required foraging rate' is double previous estimates of the maximum rates of energy acquisition for birds of this size. We suggest that the greater likelihood of a raised energy expenditure associated with larger clutches, combined with the difficulties in maintaining energy supplies, may constitute a constraint on avian clutch size.     

The energy cost of song in the canary, Serinus canaria

Although sound production requires energy, it has been unclear how much singing increases metabolic rate in passerine birds. We measured the rate of oxygen consumption of two breeds of canary that sang inside a respirometry chamber. Metabolic rate increased with the proportion of time that birds spent singing. Average metabolic rate during singing at 15-20°C was 1.05-1.07 times that of standing quietly in the same temperature range or 2.2-2.6 times basal metabolic rate (BMR). Whether an increase in metabolic rate during song of this order would represent a fitness cost to free-living passerine birds would depend upon the circumstances. Singing rather than perching during the day would raise metabolic rate only slightly. Singing at night or at dawn, instead of sleeping with a metabolic rate closer to BMR, would cause a greater increase in metabolism. Birdsong could act as a condition-dependent signal, since birds that are easily able to achieve energy balance could afford the cost of singing, but those close to their energy limits might not. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Lesions of a telencephalic nucleus in male zebra finches: Influences on vocal behavior in juveniles and adults

Male zebra finches learn to sing during a restricted phase of juvenile development. Song learning is characterized by the progressive modification of unstable song vocalizations by juvenile birds during development, a process that leads to the production of stereotyped vocal patterns as birds reach adulthood. The medial magnocellular nucleus of the anterior neostriatum (mMAN) is a small cortical region that has been implicated in song behavior based on its neuronal projection to the High Vocal Center (HVC), a nucleus that is critical for adult vocal production and presumably also plays a role in song learning. To assess the function of mMAN in song, ibotenic acid lesions of this brain region were made in juvenile male zebra finches during the period of vocal learning (40-50 days of age) and in adult males that were producing stable song (>90 days of age). Birds lesioned as juveniles produced highly abnormal, poor quality song as adults. Although the overall song quality of birds lesioned as adults was not highly disrupted or abnormal, the postoperative song behavior of these birds was discernibly different due to slight increases in variability of vocal production, particularly at the onset of singing. These results demonstrate that mMAN plays some important role in vocal production during the sensitive period for song learning, and is also important for consistent initiation and stereotyped production of adult song behavior.     

The song structure and seasonal patterns of vocal behavior of male and female bellbirds (Anthornis melanura)

The bellbird (Anthornis melanura) is a honeyeater endemic to New Zealand, which uses song to defend breeding territories and/or food resources year round. Both sexes sing and the song structure and singing behavior have not yet been quantified. The number of song types, spectral structure, repertoire size, and singing behavior of male and female bellbirds was investigated for a large island population. Song types differed between the sexes with males singing a number of structurally distinct song types and females producing song types that overlapped in structure. Singing behavior also differed between the sexes; males often sung long series of songs while females sung each song at relatively long and variable intervals. Singing by both sexes occurred year round but the frequency of male and female singing bouts showed contrasting seasonal patterns. The frequency of female singing bouts increased as the breeding season progressed, whereas male singing bouts decreased. In contrast to almost all studied passerines, female bellbirds exhibited significant singing behavior and sung songs of complex structure and variety that parallel male song. These results provide a quantitative foundation for further research of song in bellbirds and in particular the function of female vocal behavior.     

Forebrain circuits underlying the social modulation of vocal communication signals

Across vertebrate species, signalers alter the structure of their communication signals based on the social context. For example, male Bengalese finches produce faster and more stereotyped songs when directing song to females (female‐directed [FD] song) than when singing in isolation (undirected [UD] song), and such changes have been found to increase the attractiveness of a male's song. Despite the importance of such social influences, little is known about the mechanisms underlying the social modulation of communication signals. To this end, we analyzed differences in immediate early gene (EGR‐1) expression when Bengalese finches produced FD or UD song. Relative to silent birds, EGR‐1 expression was elevated in birds producing either FD or UD song throughout vocal control circuitry, including the interface nucleus of the nidopallium (NIf), HVC, the robust nucleus of the arcopallium (RA), Area X, and the lateral magnocellular nucleus of the anterior nidopallium (LMAN). Moreover, EGR‐1 expression was higher in HVC, RA, Area X, and LMAN in males producing UD song than in males producing FD song, indicating that social context modulated EGR‐1 expression in these areas. However, EGR‐1 expression was not significantly different between males producing FD or UD song in NIf, the primary vocal motor input into HVC, suggesting that context‐dependent changes could arise de novo in HVC. The pattern of context‐dependent differences in EGR‐1 expression in the Bengalese finch was highly similar to that in the zebra finch and suggests that social context affects song structure by modulating activity throughout vocal control nuclei. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 47–63, 2016     

Acoustic Monitoring Reveals Congruent Patterns of Territorial Singing Behaviour in Male and Female Tropical Wrens

Many animals defend territories against conspecific individuals using acoustic signals. In birds, male vocalizations are known to play a critical role in territory defence. Territorial acoustic signals in females have been poorly studied, perhaps because female song is uncommon in north‐temperate ecosystems. In this study, we compare male vs. female territorial singing behaviour in Neotropical rufous‐and‐white wrens Thryothorus rufalbus, a species where both sexes produce solo songs and often coordinate their songs in vocal duets. We recorded free‐living birds in Costa Rica using an eight‐microphone Acoustic Location System capable of passively triangulating the position of animals based on their vocalizations. We recorded 17 pairs of birds for 2–4 consecutive mornings and calculated the territory of each individual as a 95% fixed kernel estimate around their song posts. We compared territories calculated around male vs. female song posts, including separate analyses of solo vs. duet song posts. These spatial analyses of singing behaviour reveal that males and females use similarly sized territories with more than 60% overlap between breeding partners. Territories calculated based on solo vs. duet song posts were of similar size and similar degrees of overlap. Solos and duets were performed at similar distances from the nest for both sexes. Overall, male and female rufous‐and‐white wrens exhibit very similar spatial territorial singing behaviour, demonstrating congruent patterns of male and female territoriality.     

Raised thermoregulatory costs at exposed song posts increase the energetic cost of singing for willow warblers Phylloscopus trochilus

Sexually selected displays, such as bird song, are expected to be costly. We examined a novel potential cost to bird song: whether a less favourable microclimate at exposed song posts would be predicted to raise metabolic rate. We measured the microclimate and height at which willow warblers Phylloscopus trochilus sang and foraged. Song posts were higher than foraging sites. The wind speed was 0.6±0.3 ms⁻¹ greater at song posts (mean±SD, N=12 birds). Song rate and song post selection were not influenced consistently by temperature or wind speed, but the birds sang from lower positions on one particularly windy day. This may have resulted from difficulty in holding on to exposed branches in windy conditions rather than a thermoregulatory constraint. The results suggest that the extra thermoregulatory costs at song posts would increase metabolic rate by an average of 10±4% and a maximum of 25±8% (N=12 birds) relative to birds singing at foraging sites. We estimated that metabolic rate would be 3–8% greater during singing than during quiet respiration because of heat and evaporative water loss in exhaled gases. The combined energy requirements for sound production, thermoregulation at exposed song posts and additional heat loss in exhaled air could increase the metabolic rate of willow warblers by an average of 14–23%, and a maximum of 42–63%, during singing. The energetic cost of singing may thus be much greater for birds in a cold, windy environment than for birds singing in laboratory conditions.     

The Return of the Intruder: Immediate and Later Effects of Different Approach Distances in a Territorial Songbird

Male songbirds often maintain territories throughout the breeding season, and one of the main functions of song is to deter invaders. Therefore, the distance of an unknown singing rival should play a crucial role within territorial singing interactions of males. This distance is expected to be assessed as more threatening the closer the rival approaches. Here, we tested this assumption by conducting nocturnal playbacks from two different distances in territorial Common nightingales (Luscinia megarhynchos). Immediate vocal responses of birds were examined by analysing changes in song structure as well as temporal response features. The next morning, follow‐up playbacks from an intermediate distance allowed us to investigate longer‐lasting effects of nocturnal playbacks. We found that the distance of a simulated rival had an effect on both immediate and later vocal responses of territorial male nightingales with different song parameters being affected during nocturnal and diurnal singing. This indicates that birds perceive intruder distances and adjust their response behaviour both immediately and in later interactions.     

Male and female rufous‐and‐white wrens do not match song types with same‐sex rivals during simulated territorial intrusions

In birds with song repertoires, song‐type matching occurs when an individual responds to another individual's song by producing the same song type. Song‐type matching has been described in multiple bird species and a growing body of evidence suggests that song‐type matching may serve as a conventional signal of aggression, particularly in male birds in the temperate zone. Few studies have investigated song‐type matching in tropical birds or female birds, in spite of the fact that avian biodiversity is highest in the tropics, that female song is widespread in the tropics, and that female song is the ancestral state among songbirds. In this study of rufous‐and‐white wrens Thryophilus rufalbus, a resident neotropical songbird where both sexes sing, we presented territorial males and females with playback that simulated a territorial rival producing shared and unshared songs. In response, both males and females sang matched song types at levels statistically equal to levels expected by chance. Furthermore, males and females exhibited similar levels of aggression and similar vocal behaviours in response to playback of both shared and unshared songs. These results indicate that rufous‐and‐white wrens do not use song‐type matching in territorial conflicts as a conventional signal of aggression. We discuss alternative hypotheses for the function of song‐type sharing in tropical birds. In particular, we point out that shared songs may play an important role in intra‐pair communication, especially for birds where males and females combine their songs in vocal duets, and this may supersede the function of song‐type matching in some tropical birds.     

Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

Cost of living in free-ranging degus (Octodon degus): seasonal dynamics of energy expenditure

Animals process and allocate energy at different seasons at variable rates, depending on their breeding season and changes in environmental conditions and resulting physiological demands. Overall total energy expenditure, in turn, should either increase in some seasons due to special added demands (e.g. reproduction) or it could simply remain at about the same level, in which case the animals must show compensatory rebalancing of other expenditures that can be reduced. To test for the alternative hypotheses of seasonal variability or compensation, we measured total daily energy expenditure (DEE) in free-living degus (Octodon degus) at four seasons and followed this with determinations of basal metabolic rate (BMR) in the laboratory in the same individuals. DEE varied seasonally but was only significantly different (lower) in summer (non-breeding season), with a DEE:BMR ratio of only 1.6, whereas autumn, winter and spring DEE values were statistically indistinguishable from one another and showed DEE:BMR ratios ranging from 1.9 to 2.2. Our values of DEE in the field fall within the broad range of allometric expectation for herbivorous mammals in general, but the ratios of DEE:BMR are lower than expected. This, together with the lack of strong major shifts in total levels of DEE, suggests that degus are showing compensatory shifts among various categories of energy expenditure that allow them to manage their overall energy balance by minimizing total expenditure.     

Do females invest more into eggs when males sing more attractively? Postmating sexual selection strategies in a monogamous reed passerine

Maternal investment can play an important role for offspring fitness, especially in birds, as females have to provide their eggs with all the necessary nutrients for the development of the embryo. It is known that this type of maternal investment can be influenced by the quality of the male partner. In this study, we first verify that male song is important in the mate choice of female Eurasian reed warblers, as males mate faster when their singing is more complex. Furthermore, female egg investment varies in relation to male song characteristics. Interestingly, clutch size, egg weight, or size, which can be considered as an high‐cost investment, is not influenced by male song characteristics, whereas comparably low‐cost investment types like investment into diverse egg components are adjusted to male song characteristics. In line with this, our results suggest that female allocation rules depend on investment type as well as song characteristics. For example, egg white lysozyme is positively correlated with male song complexity. In contrast, a negative correlation exists between‐song speed and syllable repetitiveness and egg yolk weight as well as egg yolk testosterone concentration. Thus, our results suggest that female egg investment is related to male song performance in several aspects, but female investment patterns regarding various egg compounds are not simply correlated.     

The costs of singing in nightingales

The costs of singing in birds are poorly understood. One potential type of cost is a metabolic cost of singing. Previous studies have measured short-term changes in oxygen consumption associated with bouts of vocalizations, with equivocal results. In this study, I used an alternative approach to measuring the metabolic cost of singing, by measuring overnight loss of body mass, in male common nightingales, Luscinia megarhynchos, singing at night at different rates. Nightingales were shown not to forage at night. They reached a higher mass at dusk prior to singing more at night, and lost more mass overnight when dusk mass and overnight song rate were high. These results show that singing at night is associated with increased overnight consumption of body reserves, which represents a significant metabolic cost of singing at night. However, the correlation between dusk mass and overnight song rate makes it impossible to determine whether these costs arise from the energetic costs of the singing itself, or from the metabolic costs of the additional body reserves laid down at dusk on nights when song rate was high. There are also likely to be costs associated with accumulating and carrying these extra body reserves during daylight, as well as other potential costs of singing such as an increased risk of predation. These results are consistent with those models of signalling in biology that predict or assume that honest signals are costly. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Is song-type matching a conventional signal of aggressive intentions?

Song-type matching is a singing strategy found in some oscine songbirds with repertoires of song types and at least partial sharing of song types between males. Males reply to the song of a rival male by subsequently singing the same song type. For type matching to serve as an effective long-distance threat signal, it must be backed up by some probability of aggressive approach and impose some type of cost on senders that minimizes the temptation to bluff. Western subspecies of the song sparrow exhibit moderate levels of song-type sharing between adjacent males and sometimes type match in response to playback of song types they possess in their repertoires. Interactive playback experiments were used in order to examine the subsequent behaviour of type-matching birds and to quantify the responses of focal birds to type-matching versus non-matching stimuli. Birds that chose to type match the playback of a shared song type subsequently approached the speaker much more aggressively than birds that did not type match. Moreover, birds approached a type-matching stimulus much more aggressively than a non-matching stimulus. These results and consideration of alternatives suggest that type matching in song sparrows is a conventional signal in which honesty is maintained by a receiver retaliation cost against bluffers.     

Energetics of the acrobatic courtship in male golden-collared manakins (Manacus vitellinus)

In lek mating systems, females choose mates through indicators of quality, which males may exhibit by their performance of courtship displays. In temperate regions, displaying seasons are brief (one to two months), whereas in the tropics courtship seasons may be prolonged. Moreover, in temperate-breeding animals lekking behaviour can be energetically demanding, but little is known about the energy costs of lekking in tropical animals. Daily, over the course of a nearly seven-month-long breeding season, male golden-collared manakins (Manacus vitellinus) of Panamanian rainforests perform acrobatic courtship displays that markedly elevate heart rates, suggesting that they require high energy investment. Typically, animals of tropical lowland forests (such as manakins) exhibit a ‘slow pace of life’ metabolic strategy. We investigated whether male manakin courtship is indeed metabolically costly or whether the birds retain a low daily energy expenditure (DEE), as seen in other tropical species. To assess these questions, we calibrated manakin heart rate against metabolic rate, examined daily lek activity and, using telemetry, obtained heart rates of individual wild, lekking male manakins. Although metabolic rates peak during courtship displays, we found that males actually invest minimal time (only approx. 5 min d⁻¹) performing displays. As a consequence, the DEE of approximately 39 kJ d⁻¹ for male manakins is comparable to other lowland tropical species. The short, intense bursts of courtship by these birds make up only approximately 1.2% of their total DEE. Presumably, this cost is negligible, enabling them to perform daily at their arenas for months on end.     

白腰文鸟发声行为的性别差异及其机制

通过声谱分析,研究了５－１２０日龄雌、雄白腰文鸟（Lonchura striata swinhoei)的声谱变化,及该时段３个主要发声控制核团）ＨＶＣ、ＲＡ、Ａrea X)体积、睾丸（睾酮）的相应改变。结果如下：①４５日龄以前,雌雄鸟只能发出简单鸣叫（call),鸣声基本不会鸣唱。②雄性ＨＶＣ,ＲＡ,ＡreaX体积均比雌性大２－６部。３个核团的大小发育不完全一致。各核团的快速生长期与鸣唱学习的主要时段（６０－１２０日龄）不同步,说明核团的个体发育可能不完全受发声行为的影响。③睾丸的充分发育（１２０日龄后）及血液中具有较高的睾酮水平是雄鸟发出成熟鸣唱语句的重要条件。     

Metabolic and respiratory costs of increasing song amplitude in zebra finches

Bird song is a widely used model in the study of animal communication and sexual selection, and several song features have been shown to reflect the quality of the singer. Recent studies have demonstrated that song amplitude may be an honest signal of current condition in males and that females prefer high amplitude songs. In addition, birds raise the amplitude of their songs to communicate in noisy environments. Although it is generally assumed that louder song should be more costly to produce, there has been little empirical evidence to support this assumption. We tested the assumption by measuring oxygen consumption and respiratory patterns in adult male zebra finches (Taeniopygia guttata) singing at different amplitudes in different background noise conditions. As background noise levels increased, birds significantly increased the sound pressure level of their songs. We found that louder songs required significantly greater subsyringeal air sac pressure than quieter songs. Though increased pressure is probably achieved by increasing respiratory muscle activity, these increases did not correlate with measurable increases in oxygen consumption. In addition, we found that oxygen consumption increased in higher background noise, independent of singing behaviour. This observation supports previous research in mammals showing that high levels of environmental noise can induce physiological stress responses. While our study did not find that increasing vocal amplitude increased metabolic costs, further research is needed to determine whether there are other non-metabolic costs of singing louder or costs associated with chronic noise exposure.     

Reward Associated with Singing Behavior Correlates with Opioid-Related Gene Expression in the Medial Preoptic Nucleus in Male European Starlings

Birdsong consists of species-specific learned vocal sequences that are used primarily to attract mates and to repel competitors during the breeding season. However, many birds continue to sing at times when vocal production has no immediate or obvious impact on conspecific behavior. The mechanisms that ensure that animals produce important behaviors in contexts in which the function of these behaviors is not immediate or obvious are not known. One possibility is that animals engage in such behaviors because they are associated with pleasure. Here we examined the hypothesis that male European starlings sing outside of the breeding season in part because the act of singing in this context is facilitated and/or maintained by opioid-mediated reward. We measured song-associated reward using a conditioned place preference (CPP) test in male starlings producing fall, non-breeding season-typical song. We used quantitative real time PCR to measure expression of the enkephalin opioid precursor preproenkephalin (PENK) and mu opioid receptors (MOR) in the medial preoptic nucleus (POM; a region in which opioids are implicated in both reward and starling fall song) and additionally the song control region HVC as a control. Starlings developed a strong preference for a place that had been paired previously with the act of producing fall-typical song, indicating that fall song production was associated with a positive affective state. Both PENK and MOR mRNA expression in the POM, but not HVC, correlated positively with both individual reward state (as reflected in CPP) and undirected singing behavior. These results suggest that singing induces opioid receptor and enkephalin expression in the POM and consequent reward, and/or that opioid release in the POM induced by individual or environmental factors (e.g., the presence of food, safety of a flock or the absence of predators) induces a positive affective state which then facilitates singing behavior.     

Variation in singing style use in the reed bunting Emberiza schoeniclus: influencing factors and possible functions

The two main functions of bird song are territory defence and mate attraction. Considerable progress has been made in understanding how species adjust the use of songs to serve these and other (presumed) functions of bird song, but the striking variety of singing behavior observable in wild birds remains enigmatic. Some species make do with simple songs and small repertoires, while others show large, complex repertoires and still others have evolved several distinct singing styles. In most species with distinct singing styles, however, the functions of singing styles are poorly understood. Two distinct singing styles (type I and II, respectively) have long been known in the reed bunting Emberiza schoeniclus, while a new third one has recently been reported to exist. We first quantitatively investigated the evidence for the existence of three singing styles. Then, we tested predictions of the mate attraction hypothesis, the mate guarding hypothesis and the territory defence hypothesis by examining the relations between singing style use with social and temporal factors. Cluster and discriminant analyses supported the existence of three (instead of two) singing styles, which could be differentiated based on four variables referring to song structure and complexity. Use of singing styles was related to male mating status (consistent with the mate attraction hypothesis), but not to female breeding stage (no support for the mate guarding hypothesis). Finally, use of singing styles differed in relation to time of day, with the dawn chorus of paired reed buntings consisting almost exclusively of songs of the recently discovered type III singing style and daytime singing primarily consisting of songs of long‐known type I (in unpaired males) or II singing styles (in paired males). Our findings suggest that one singing style (type I) primarily serves to attract a social mate, although an additional territorial function of this singing style cannot be dismissed. The function(s) of the other two singing styles, both only sung by paired males, are not related to attraction of a social mate or to the own female's fertility, but appear to be important in the context of territory defence and extra‐pair matings.