Insectivorous birds can see and smell systemically herbivore-induced pines.

Several studies have shown that insectivorous birds are attracted to herbivore-damaged trees even when they cannot see or smell the actual herbivores or their feces. However, it often remained an open question whether birds are attracted by herbivore-induced changes in leaf odor or in leaf light reflectance or by both types of changes. Our study addressed this question by investigating the response of great tits (Parus major) and blue tits (Cyanistes caeruleus) to Scots pine (Pinus sylvestris) damaged by pine sawfly larvae (Diprion pini). We released the birds individually to a study booth, where they were simultaneously offered a systemically herbivore-induced and a noninfested control pine branch. In the first experiment, the birds could see the branches, but could not smell them, because each branch was kept inside a transparent, airtight cylinder. In the second experiment, the birds could smell the branches, but could not see them, because each branch was placed inside a nontransparent cylinder with a mesh lid. The results show that the birds were more attracted to the herbivore-induced branch in both experiments. Hence, either type of the tested cues, the herbivore-induced visual plant cue alone as well as the olfactory cues per se, is attractive to the birds.

Insectivorous Birds Are Attracted by Plant Traits Induced by Insect Egg Deposition.

Insectivorous birds feed upon all developmental stages of herbivorous insects, including insect eggs if larvae and adults are unavailable. Insect egg deposition on plants can induce plant traits that are subsequently exploited by egg parasitoids searching for hosts. However, it is unknown whether avian predators can also use egg-induced plant changes for prey localization. Here, we studied whether great tits (Parus major) and blue tits (Cyanistes caeruleus) are attracted by traits of the Scots pine (Pinus sylvestris) induced by pine sawfly (Diprion pini) egg deposition. We chose this plant - insect system because sawfly egg deposition on pine needles is known to locally and systemically induce a change in pine volatile organic compounds (VOCs), and tits are known to prey upon sawfly eggs. In dual choice laboratory experiments, we simultaneously offered the birds an egg-free control branch and a systemically egg-induced branch. Significantly more birds visited the egg-induced branch first. We confirmed by GC-MS analyses that systemically egg-induced branches released more (E)-ß-farnesene compared to control branches. Spectrophotometric analyses showed that control branches reflected more light than egg-induced branches throughout the avian visual range. Although a discrimination threshold model for blue tits suggests that the birds are poor at discriminating this visual difference, the role of visual stimuli in attracting the birds to egg-induced pines cannot be discounted. Our study shows, for the first time, that egg-induced odorous and/or visual plant traits can help birds to locate insect eggs without smelling or seeing those eggs.

Affairs happen-to whom? A study on extrapair paternity in common nightingales.

Most birds engage in extrapair copulations despite great differences across and within species. Besides cost and benefit considerations of the two sex environmental factors have been found to alter mating strategies within or between populations and/or over time. For socially monogamous species, the main advantage that females might gain from mating with multiple males is probably increasing their offspring's genetic fitness. Since male (genetic) quality is mostly not directly measurable for female birds, (extrapair) mate choice is based on male secondary traits. In passerines male song is such a sexual ornament indicating male phenotypic and/or genetic quality and song repertoires seem to affect female mate choice in a number of species. Yet their role in extrapair mating behavior is not well understood. In this study, we investigated the proportion of extrapair paternity (EPP) in a population of common nightingales Luscinia megarhynchos. We found that EPP rate was rather high (21.5% of all offspring tested) for a species without sexual dimorphism and high levels of paternal care. Furthermore, the occurrence of EPP was strongly related to the spatial distribution of male territories with males settling in densely occupied areas having higher proportions of extrapair young within their own brood. Also, song repertoire size affected EPP: here larger repertoires of social mates were negatively related to the probability of being cuckolded. When directly comparing repertoires sizes of social and extrapair mates, extrapair mates tended to have larger repertoires. We finally discuss our results as a hint for a flexible mating strategy in nightingales where several factors-including ecological as well as male song features-need to be considered when studying reproductive behavior in monogamous species with complex song.

Early developmental stress negatively affects neuronal recruitment to avian song system nucleus HVC.

Adverse environmental conditions can impact the life history trajectory of animals. Adaptive responses enable individuals to cope with unfavorable conditions, but altered metabolism and resource allocation can bear long-term costs. In songbirds, early developmental stress can cause lifelong changes in learned song, a culturally transmitted trait, and nestlings experiencing developmental stress develop smaller song control nucleus HVCs. We investigated whether nutrition-related developmental stress impacts neurogenesis in HVC, which may explain how poor nutrition leads to smaller HVC volume. We provided different quality diets (LOW and HIGH) by varying the husks-to-seeds ratio to zebra finch families for the first 35 days after the young hatched (PHD). At PHD14-18 and again at nutritional independence (PHD35), juveniles were injected with different cell division markers. To monitor growth, we took body measures at PHD10, 17, and 35. At PHD35 the number of newly recruited neurons in HVC and the rate of proliferation in the adjacent ventricular zone (VZ) were counted. Males raised on the LOW diet for their first weeks of life had significantly fewer new neurons in HVC than males raised on the HIGH diet. At the time when these new HVC neurons were born and labeled in the VZ (PHD17) the birds exposed to the LOW diet had significantly lower body mass. At PHD35 body mass or neuronal proliferation no longer differed. Our study shows that even transitory developmental stress can have negative consequences on the cellular processes underlying the development of neural circuits.

Multiple song features are related to paternal effort in common nightingales.

BACKGROUND: Sexual ornamentation may be related to the degree of paternal care and the 'good-parent' model predicts that male secondary characters honestly advertise paternal investment. In most birds, males are involved in bringing up the young and successful reproduction highly depends on male contribution during breeding. In passerines, male song is indicative of male attributes and for few species it has been shown that song features also signal paternal investment to females. Males of nightingales Luscinia megarhynchos are famous for their elaborate singing but so far there is only little knowledge on the role of male song in intersexual communication, and it is unknown whether male song predicts male parenting abilities. RESULTS: Using RFID technology to record male feeding visits to the nest, we found that nightingale males substantially contribute to chick feeding. Also, we analyzed male nocturnal song with focus on song features that have been shown to signal male quality before. We found that several song features, namely measures of song complexity and song sequencing, were correlated with male feeding rates. Moreover, the combination of these song features had strong predictive power for male contribution to nestling feeding. CONCLUSIONS: Since male nightingales are involved in chick rearing, paternal investment might be a crucial variable for female mate choice in this species. Females may assess future paternal care on the basis of song features identified in our study and thus these features may have evolved to signal direct benefits to females. Additionally we underline the importance of multiple acoustic cues for female mating decisions especially in species with complex song such as the nightingale.

The use of network analysis to study complex animal communication systems: a study on nightingale song.

The singing of song birds can form complex signal systems comprised of numerous subunits sung with distinct combinatorial properties that have been described as syntax-like. This complexity has inspired inquiries into similarities of bird song to human language; but the quantitative analysis and description of song sequences is a challenging task. In this study, we analysed song sequences of common nightingales (Luscinia megarhynchos) by means of a network analysis. We translated long nocturnal song sequences into networks of song types with song transitions as connectors. As network measures, we calculated shortest path length and transitivity and identified the 'small-world' character of nightingale song networks. Besides comparing network measures with conventional measures of song complexity, we also found a correlation between network measures and age of birds. Furthermore, we determined the numbers of in-coming and out-going edges of each song type, characterizing transition patterns. These transition patterns were shared across males for certain song types. Playbacks with different transition patterns provided first evidence that these patterns are responded to differently and thus play a role in singing interactions. We discuss potential functions of the network properties of song sequences in the framework of vocal leadership. Network approaches provide biologically meaningful parameters to describe the song structure of species with extremely large repertoires and complex rules of song retrieval.

The causes and evolutionary consequences of mixed singing in two hybridizing songbird species (Luscinia spp.).

Bird song plays an important role in the establishment and maintenance of prezygotic reproductive barriers. When two closely related species come into secondary contact, song convergence caused by acquisition of heterospecific songs into the birds' repertoires is often observed. The proximate mechanisms responsible for such mixed singing, and its effect on the speciation process, are poorly understood. We used a combination of genetic and bioacoustic analyses to test whether mixed singing observed in the secondary contact zone of two passerine birds, the Thrush Nightingale (Luscinia luscinia) and the Common Nightingale (L. megarhynchos), is caused by introgressive hybridization. We analysed song recordings of both species from allopatric and sympatric populations together with genotype data from one mitochondrial and seven nuclear loci. Semi-automated comparisons of our recordings with an extensive catalogue of Common Nightingale song types confirmed that most of the analysed sympatric Thrush Nightingale males were 'mixed singers' that use heterospecific song types in their repertoires. None of these 'mixed singers' possessed any alleles introgressed from the Common Nightingale, suggesting that they were not backcross hybrids. We also analysed songs of five individuals with intermediate phenotype, which were identified as F1 hybrids between the Thrush Nightingale female and the Common Nightingale male by genetic analysis. Songs of three of these hybrids corresponded to the paternal species (Common Nightingale) but the remaining two sung a mixed song. Our results suggest that although hybridization might increase the tendency for learning songs from both parental species, interspecific cultural transmission is the major proximate mechanism explaining the occurrence of mixed singers among the sympatric Thrush Nightingales. We also provide evidence that mixed singing does not substantially increase the rate of interspecific hybridization and discuss the possible adaptive value of this phenomenon in nightingales.

Life-history and hormonal control of aggression in black redstarts: Blocking testosterone does not decrease territorial aggression, but changes the emphasis of vocal behaviours during simulated territorial intrusions.

INTRODUCTION: Many studies in behavioural endocrinology attempt to link territorial aggression with testosterone, but the exact relationship between testosterone and territorial behaviour is still unclear and may depend on the ecology of a species. The degree to which testosterone facilitates territorial behaviour is particularly little understood in species that defend territories during breeding and outside the breeding season, when plasma levels of testosterone are low. Here we suggest that species that defend territories in contexts other than reproduction may have lost the direct regulation of territorial behaviour by androgens even during the breeding season. In such species, only those components of breeding territoriality that function simultaneously as sexually selected signals may be under control of sex steroids. RESULTS: We investigated black redstarts (Phoenicurus ochruros), a species that shows periods of territoriality within and outside of the breeding season. We treated territorial males with an anti-androgen and an aromatase inhibitor during the breeding season to block both the direct and indirect effects of testosterone. Three and ten days after the treatment, implanted males were challenged with a simulated territorial intrusion. The treatment did not reduce the overall territorial response, but it changed the emphasis of territoriality: experimental males invested more in behaviours addressed directly towards the intruder, whereas placebo-treated males put most effort into their vocal response, a component of territoriality that may be primarily directed towards their mating partner rather than the male opponent. CONCLUSIONS: In combination with previous findings, these data suggest that overall territoriality may be decoupled from testosterone in male black redstarts. However, high levels of testosterone during breeding may facilitate-context dependent changes in song.

Associated and disassociated patterns in hormones, song, behavior and brain receptor expression between life-cycle stages in male black redstarts, Phoenicurus ochruros.

Testosterone has been suggested to be involved in the regulation of male territorial behavior. For example, seasonal peaks in testosterone typically coincide with periods of intense competition between males for territories and mating partners. However, some species also express territorial behavior outside a breeding context when testosterone levels are low and, thus, the degree to which testosterone facilitates territorial behavior in these species is not well understood. We studied territorial behavior and its neuroendocrine correlates in male black redstarts. Black redstarts defend territories in spring during the breeding period, but also in the fall outside a reproductive context when testosterone levels are low. In the present study we assessed if song output and structure remain stable across life-cycle stages. Furthermore, we assessed if brain anatomy may give insight into the role of testosterone in the regulation of territorial behavior in black redstarts. We found that males sang spontaneously at a high rate during the nonbreeding period when testosterone levels were low; however the trill-like components of spontaneously produced song contained less repetitive elements during nonbreeding than during breeding. This higher number of repetitive elements in trills did not, however, correlate with a larger song control nucleus HVC during breeding. However, males expressed more aromatase mRNA in the preoptic area - a brain nucleus important for sexual and aggressive behavior - during breeding than during nonbreeding. In combination with our previous studies on black redstarts our results suggest that territorial behavior in this species only partly depends on sex steroids: spontaneous song output, seasonal variation in trills and non-vocal territorial behavior in response to a simulated territorial intruder seem to be independent of sex steroids. However, context-dependent song during breeding may be facilitated by testosterone - potentially by conversion of testosterone to estradiol in the preoptic area.

Buzzwords in females' ears? The use of buzz songs in the communication of nightingales (Luscinia megarhynchos).

Differences in individual male birds' singing may serve as honest indicators of male quality in male-male competition and female mate choice. This has been shown e.g. for overall song output and repertoire size in many bird species. More recently, differences in structural song characteristics such as the performance of physically challenging song components were analysed in this regard. Here we show that buzz elements in the song of nightingales (Luscinia megarhynchos) hold the potential to serve as indicators of male quality and may therefore serve a communicative function. Buzzes were produced with considerable differences between males. The body weight of the males was correlated with one measure of these buzzes, namely the repetition rate of the buzz subunits, and individuals with larger repertoires sang buzzes at higher subunit-rates. A model of buzz performance constraints suggested that buzzes were sung with different proficiencies. In playback experiments, female nightingales showed more active behaviour when hearing buzz songs. The results support the idea that performance differences in the acoustic fine structure of song components are used in the communication of a large repertoire species such as the nightingale.

Testosterone affects song modulation during simulated territorial intrusions in male black redstarts (Phoenicurus ochruros).

Although it has been suggested that testosterone plays an important role in resource allocation for competitive behavior, details of the interplay between testosterone, territorial aggression and signal plasticity are largely unknown. Therefore, we investigated if testosterone acts specifically on signals that communicate the motivation or ability of individuals to engage in competitive situations in a natural context. We studied the black redstart, a territorial songbird species, during two different life-cycle stages, the early breeding phase in spring and the non-breeding phase in fall. Male territory holders were implanted with the androgen receptor blocker flutamide (Flut) and the aromatase inhibitor letrozole (Let) to inhibit the action of testosterone and its estrogenic metabolites. Controls received a placebo treatment. Three days after implantation birds were challenged with a simulated territorial intrusion (STI). Song was recorded before, during and after the challenge. In spring, both treatment groups increased the number of elements sung in parts of their song in response to the STI. However, Flut/Let-implanted males reacted to the STI with a decreased maximum acoustic frequency of one song part, while placebo-implanted males did not. Instead, placebo-implanted males sang the atonal part of their song with a broader frequency range. Furthermore, placebo-, but not Flut/Let-implanted males, sang shorter songs with shorter pauses between parts in the STIs. During simulated intrusions in fall, when testosterone levels are naturally low in this species, males of both treatment groups sang similar to Flut/Let-implanted males during breeding. The results suggest that song sung during a territorial encounter is of higher competitive value than song sung in an undisturbed situation and may, therefore, convey information about the motivation or quality of the territory holder. We conclude that testosterone facilitates context-dependent changes in song structures that may be honest signals of male quality in black redstarts.

Does age matter in song bird vocal interactions? Results from interactive playback experiments.

The song of oscines provides an extensively studied model of age-dependent behaviour changes. Male and female receivers might use song characteristics to obtain information about the age of a signaller, which is often related to its quality. Whereas most of the age-dependent song changes have been studied in solo singing, the role of age in vocal interactions is less well understood. We addressed this issue in a playback study with common nightingales (Luscinia megarhynchos). Previous studies showed that male nightingales had smaller repertoires in their first year than older males and males adjusted their repertoire towards the most common songs in the breeding population. We now compared vocal interaction patterns in a playback study in 12 one year old and 12 older nightingales (cross-sectional approach). Five of these males were tested both in their first and second breeding season (longitudinal approach). Song duration and latency to respond did not differ between males of different ages in either approach. In the cross-sectional approach, one year old nightingales matched song types twice as often as did older birds. Similarly, in the longitudinal approach all except one bird reduced the number of song type matches in their second season. Individuals tended to overlap songs at higher rates in their second breeding season than in their first. The higher levels of song type matches in the first year and song overlapping by birds in their second year suggest that these are communicative strategies to establish relationships with competing males and/or choosy females.

Do Barbary macaques 'comment' on what they see? A first report on vocalizations accompanying interactions of third parties.

Primates acquire knowledge about relationships of third parties and group structure by monitoring their conspecifics. We show that Barbary macaques (Macaca sylvanus) utter specific vocalizations while monitoring interactions of other group members. As they did not direct other behaviours to the interacting group members, we provisionally termed these vocalizations 'vocal comments'. We investigated the acoustic properties of these comments and the social contexts in which they occurred. Most adult males and females of two studied groups produced low-amplitude calls when observing close contact interactions of other group members. The acoustic features of these calls varied with characteristics of the commented situation. Our results suggest that such calls might not be directed towards the agents of the commented situation, but towards other group members. The vocal comments may signal the caller's awareness of the observed interaction and possibly attract the attention of others to the situation.

Dynamic-acoustic variation causes differences in evaluations of laughter.

Exposure to laughter has striking effects on human listeners and may facilitate positive emotional and behavioural responses. The acoustic signal pattern of laughter vocalisations is particularly suitable to elicit these reactions. However, little is known about factors that lead to differences in reactions of listeners. The acoustic quality of laughter, the social context, and the disposition of the listener are possible variables in differences in evaluation. We conducted experiments using playback techniques in which human laughter elicited in a natural setting was evaluated by listeners (N=90). Listeners evaluated several phrases of laughter produced by different laughing targets. We investigated the role of the characteristics of voice, dynamic-acoustic characteristics, and order of playback sequence on the evaluation of laughter. The dynamic-acoustic characteristics of laughter significantly affected evaluations by listeners, whereas voice and the playback order did not. An acoustic analysis allowed us to identify acoustic parameters that contribute to such differences in evaluation.

The use of vocal signals in the social play of barbary macaques.

Field studies in various species of Macaca (Cercopithecidae) provided evidence for specific visual displays that typically accompany playful interactions. The aim of our study was to examine whether and when playing individuals would use auditory displays, i.e. vocalizations that often occur during social play as well. The study was conducted on a population of semi-free Barbary macaques (Macaca sylvanus) with a special focus on the composition and dynamics of playful wrestling (synonymous term: 'rough-and-tumble play'). Analyses of dyadic encounters between subadult males allowed us to distinguish five types of playful behaviours and three types of vocalizations. The latter were clearly linked to encounters where effects of visual signals were impaired, e.g. during close body contact. During wrestling, vocalizations tended to increase in the beginning of an encounter, whereas the last seconds of wrestling often showed a decline in vocalization rate. Our results allowed us to conclude that these vocalizations may supplement or in many cases even substitute interactional effects of visual signals, e.g. the 'play face.'