Sneaky copulations by subordinate males suggest direct fitness benefits from male–male associations in spotted bowerbirds (Ptilonorhynchus maculatus)

Male spotted bowerbirds (Ptilonorhynchus maculatus) build and defend a structure of sticks and straw—the bower—decorated with colourful objects to attract mates during the breeding season. Specific non-territorial, subordinate males are tolerated by resident males at bowers over multiple breeding seasons. Prior research showed that these male–male associations exhibit attributes of coalitionary behaviour and that subordinate males gain delayed benefits from associating with bower owners, namely future bower inheritance. Yet, it remained unclear whether subordinate males may additionally gain direct fitness benefits from attending established bowers. Here, we report on four separate instances of sneaky copulations (or attempts of copulating) by subordinate males at resident males' bowers. Multiple non-resident males disrupted the ongoing copulations between the bower owner and a receptive female, and these events were followed by violent aggressive interactions. These observations shed new light on same-sex social dynamics in spotted bowerbirds and support the hypothesis that subordinate males are sexually mature individuals that occasionally obtain access to females while attending established bowers. We discuss these findings in light of the literature on male courtship coalitions and agonistic behaviour in bowerbirds, and highlight further aspects of subordinate behaviour that require empirical investigation.     

Context-dependent vocal mimicry in a passerine bird

How do birds select the sounds they mimic, and in what contexts do they use vocal mimicry? Some birds show a preference for mimicking other species' alarm notes, especially in situations when they appear to be alarmed. Yet no study has demonstrated that birds change the call types they mimic with changing contexts. We found that greater racket-tailed drongos (Dicrurus paradiseus) in the rainforest of Sri Lanka mimic the calls of predators and the alarm-associated calls of other species more often than would be expected from the frequency of these sounds in the acoustic environment. Drongos include this alarm-associated mimicry in their own alarm vocalizations, while incorporating other species' songs and contact calls in their own songs. Drongos show an additional level of context specificity by mimicking other species' ground predator-specific call types when mobbing. We suggest that drongos learn other species' calls and their contexts while interacting with these species in mixed flocks. The drongos' behaviour demonstrates that alarm-associated calls can have learned components, and that birds can learn the appropriate usage of calls that encode different types of information.     

Vocal mimicry in male bowerbirds: who learns from whom?

Vocal mimicry is one of the more striking aspects of avian vocalization and is widespread across songbirds. However, little is known about how mimics acquire heterospecific and environmental sounds. We investigated geographical and individual variation in the mimetic repertoires of males of a proficient mimic, the spotted bowerbird Ptilonorhynchus maculatus. Male bower owners shared more of their mimetic repertoires with neighbouring bower owners than with more distant males. However, interbower distance did not explain variation in the highly repeatable renditions given by bower owners of two commonly mimicked species. From the similarity between model and mimic vocalizations and the patterns of repertoire sharing among males, we suggest that the bowerbirds are learning their mimetic repertoire from heterospecifics and not from each other.     

Patterns of painting in satin bowerbirds Ptilonorhynchus violaceus and males’ responses to changes in their paint

Satin bowerbirds Ptilonorhynchus violaceus have an elaborate multi‐component sexual display, some components of which have been extensively studied. We describe a relatively unstudied component of this display, bower painting, and birds’ responses to manipulations of their paint. Males of this species focus their display around a stick bower constructed on the forest floor which they decorate with a variety of objects and paint. Painting involves a male masticating plant material and wiping the plant‐saliva mixture onto the inside walls of the bower; during courtship visits to bowers, females nibble at this paint. We found that 93% of 53 males painted their bowers at our study site and the time males spent painting their bowers accounted for 24% of their time at the bower. We experimentally removed and added paint to bowers to test whether males respond to these changes in their paint. Males gave more advertisement calls and spent less time manipulating sticks at the bower when we added fresh wet paint to their bowers compared to older dried paint or a control treatment. They did not respond to the removal of paint from their bowers, perhaps because it was primarily older dried paint that was removed. We also found that males painted more frequently when there was measurable wind in their bowers, which could have degraded the quality of the signal. Our findings indicate that fresh wet paint is more important to males than older dried paint and, together with previous work at this site, suggest that paint may act as a signal to females. Given that females nibble bower sticks during courtship, we suggest that bower paint may function as a chemical sexual signal rather than a visual signal.     

Patterns of painting in satin bowerbirds Ptilonorhynchus violaceus and males' responses to changes in their paint

Satin bowerbirds Ptilonorhynchus violaceus have an elaborate multi-component sexual display, some components of which have been extensively studied. We describe a relatively unstudied component of this display, bower painting, and birds' responses to manipulations of their paint. Males of this species focus their display around a stick bower constructed on the forest floor which they decorate with a variety of objects and paint. Painting involves a male masticating plant material and wiping the plant-saliva mixture onto the inside walls of the bower; during courtship visits to bowers, females nibble at this paint. We found that 93% of 53 males painted their bowers at our study site and the time males spent painting their bowers accounted for 24% of their time at the bower. We experimentally removed and added paint to bowers to test whether males respond to these changes in their paint. Males gave more advertisement calls and spent less time manipulating sticks at the bower when we added fresh wet paint to their bowers compared to older dried paint or a control treatment. They did not respond to the removal of paint from their bowers, perhaps because it was primarily older dried paint that was removed. We also found that males painted more frequently when there was measurable wind in their bowers, which could have degraded the quality of the signal. Our findings indicate that fresh wet paint is more important to males than older dried paint and, together with previous work at this site, suggest that paint may act as a signal to females. Given that females nibble bower sticks during courtship, we suggest that bower paint may function as a chemical sexual signal rather than a visual signal.     

Feather stealing in the satin bowerbird (Ptilonorhynchus violaceus): male competition and the quality of display

Male satin bowerbirds use feathers to decorate their bowers and often steal feathers and other decorations from the bowers of other males. Decorations are a key element in sexual display and tracking their movement between bowers provides the first detailed information about this unique pattern of sexual competition. For two field seasons the movement of marked feathers was followed. Males varied greatly in stealing activity. The most active feather thieves were often from areas where bowers were close together and they were involved in reciprocal stealing with males at adjacent bowers. The rate of stealing by males was significantly correlated with the number of feathers on their bowers. This suggests that stealing is important in determining the level of bower decoration and mating success. Patterns of stealing behaviour support models of sexual selection which suggest that male interactions are important in influencing female choice through their effect on the quality of male display.     

Avian vocal mimicry: a unified conceptual framework

Mimicry is a classical example of adaptive signal design. Here, we review the current state of research into vocal mimicry in birds. Avian vocal mimicry is a conspicuous and often spectacular form of animal communication, occurring in many distantly related species. However, the proximate and ultimate causes of vocal mimicry are poorly understood. In the first part of this review, we argue that progress has been impeded by conceptual confusion over what constitutes vocal mimicry. We propose a modified version of Vane‐Wright's (1980) widely used definition of mimicry. According to our definition, a vocalisation is mimetic if the behaviour of the receiver changes after perceiving the acoustic resemblance between the mimic and the model, and the behavioural change confers a selective advantage on the mimic. Mimicry is therefore specifically a functional concept where the resemblance between heterospecific sounds is a target of selection. It is distinct from other forms of vocal resemblance including those that are the result of chance or common ancestry, and those that have emerged as a by‐product of other processes such as ecological convergence and selection for large song‐type repertoires. Thus, our definition provides a general and functionally coherent framework for determining what constitutes vocal mimicry, and takes account of the diversity of vocalisations that incorporate heterospecific sounds. In the second part we assess and revise hypotheses for the evolution of avian vocal mimicry in the light of our new definition. Most of the current evidence is anecdotal, but the diverse contexts and acoustic structures of putative vocal mimicry suggest that mimicry has multiple functions across and within species. There is strong experimental evidence that vocal mimicry can be deceptive, and can facilitate parasitic interactions. There is also increasing support for the use of vocal mimicry in predator defence, although the mechanisms are unclear. Less progress has been made in explaining why many birds incorporate heterospecific sounds into their sexual displays, and in determining whether these vocalisations are functionally mimetic or by‐products of sexual selection for other traits such as repertoire size. Overall, this discussion reveals a more central role for vocal mimicry in the behavioural ecology of birds than has previously been appreciated. The final part of this review identifies important areas for future research. Detailed empirical data are needed on individual species, including on the structure of mimetic signals, the contexts in which mimicry is produced, how mimicry is acquired, and the ecological relationships between mimic, model and receiver. At present, there is little information and no consensus about the various costs of vocal mimicry for the protagonists in the mimicry complex. The diversity and complexity of vocal mimicry in birds raises important questions for the study of animal communication and challenges our view of the nature of mimicry itself. Therefore, a better understanding of avian vocal mimicry is essential if we are to account fully for the diversity of animal signals.     

Preferences for coloured bower decorations can be explained in a nonsexual context

The sensory bias model of sexual selection suggests that elaborate male secondary sexual traits evolved to exploit biases in the female's sensory system. Such biases may have evolved in a nonsexual context. Male bowerbirds build and decorate elaborate structures, bowers, which function as targets of female choice. The colour of decorations used on bowers appears to be important in determining a male's mating success. We tested two predictions made by the sensory bias model, using cache presentation experiments of artificially coloured grapes made to captive bowerbirds of five species. We first searched for evidence of ancestral biases for certain colours that could explain current colour preferences across species. We found no single parsimonious explanation for ancestral patterns of colour preference across the family. We next tested whether female preference patterns could be explained in a nonsexual, foraging, context. For both of the species where sufficient data could be collected, female foraging preferences for grapes were significantly related to male preferences for grapes used as bower decorations. Our results suggest that choice of bower decoration colour may have evolved to exploit a bias in the female's sensory system, originally shaped by selection on foraging practices. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Sex, bowers and brains

Inter- and intraspecific variations in the sizes of specific avian brain regions correspond to the complexity of the behaviour that they govern. However, no study has demonstrated a relationship between gross brain size and behavioural complexity, a hypothesis that has been proposed to explain the unusually large human brain. I show, using X-rays of museum specimens, that species of bowerbirds that build bowers have relatively larger brains than both related and ecologically similar but unrelated species that do not build bowers. Bower design varies across species from simple cleared courts to ornate, hut-like structures large enough to contain a small child. Furthermore, species building more complex bowers have relatively larger brains, both within each of the two different bower-building clades and across the family as a whole, controlling for phylogeny. Such gross differences in brain size are surprising and may reflect the range of cognitive processes necessary for successful bower building, The relationships are strongest for males, the bower-building sex, although there is a similar trend in females. Because the size and complexity of bower design is targeted by female choice, the observation that relative brain size is related to bower complexity suggests that sexual selection may drive gross brain enlargement.     

Stealing behavior and the maintenance of a visual display in the satin bowerbird

Honest signals that indicate male quality have been observedin many species and are thought to have evolved to allow malesto assess rivals accurately and respond to "cheaters." Femalescould potentially also use the same honest signals as reliableindicators of male quality. In bowerbirds, the numbers of specificbower decorations may serve as an honest signal of male quality:this study investigates whether decoration stealing among malesatin bowerbirds at the Bunya Mountains, Australia, may alsoinvolve honest signals. In this study, we aimed to determine1) predictors for the degree to which individual male satinbowerbirds steal, and are stolen from, and 2) predictors forwhy some male pairs interact by stealing, whereas other pairsdo not. We also assessed how experimentally standardizing thenumber of decorations on bowers would affect the 1) frequencyof stealing, 2) specific interactions among males, and 3) distributionof decorations across bowers. Bower decorations were labeledand tracked through one breeding season. Males that were successfulstealers, stole from other successful stealers, had many feathersand bottle tops on their bowers and painted their bower wallsoften. Male pairs were more likely to interact by stealing iftheir bowers were in close proximity. Most of the stealing observedwas of a reciprocal nature. After we standardized the numbersand types of decorations on a small group of males' bowers,the mean number of daily stealing gains and the total numberof males interacting by stealing did not change. In addition,no significant novel stealing interactions were initiated afterthe manipulation. The average number of all bower decorationsand the average number of rosella feathers on a given male'sbower prior to the manipulation were proportional to the averagenumbers for the period after the manipulation. Furthermore,males that originally had better collections of decorationstended to suffer fewer losses due to stealing after the manipulation.Our results suggest that the total number of decorations, thetotal number of rosella feathers on a male's bower, and possiblystealing behavior, may form part of the basis of an honest signalindicating male quality and therefore might be correlated withmating success.     

Cichlid spawning structures – bowers or nests?

Males of mouthbrooding cichlids build sand-castle or sand-scrape structures. These are used as display sites to attract females, eggs are laid and inseminated there and then taken away by the female for brooding elsewhere. It has been suggested that the structure be called a bower because it has the same role as the bowerbird's bower. Thew word bower is restricted in ornithological literature to complex structures which reminded Gould (1840) of garden bowers. Simpler display sites of other bowerbirds and other bird families are called courts. Bowerbirds use separate nests for egg-laying, cichlids do not. Other birds, e.g. many weavers, use nests for display purposes. The cichlid structure is the same as nests used by other non mouthbrooding fishes, but mouthbrooding has freed females from the need to stay in the nest. It is unacceptable to use the word bower for the cichlid structure because it is not a bower as defined in ornithological literature, and it is used for egg laying as well as display. Weaver birds use nests for display in a similar way to cichlids, thus the word nest should be retained for the cichlid sand structure. This revised version was published online in July 2006 with corrections to the Cover Date.     

Tactic for bower acquisition by male cichlids,Cyathopharynx furcifer,in Lake Tanganyika

A tactic for bower acquisition by male cichlids,Cyathopharynx furcifer, was studied in Lake Tanganyika. Males held crater-shaped bowers of sand within their territories, which were located adjacent to each other. Females visited bowers to spawn eggs, subsequently brooding the eggs in their mouths. Some individuals held territories without bowers near those of males with bowers. Although only the males with bowers succeeded in reproduction, they were apparently exhausted by bower maintenance and reproduction, and often deserted their bowers. These were soon occupied by males which had held nearby territories without bowers, such males then engaging in reproductive activity. Although the construction of new bowers by males was observed, such was unsuccessful, probably because too much energy was required and/or the optimal space for bowers was limited. Direct aggression by males without bowers against bower-holding males to deprive the bowers was not observed, possibly due to the high costs of such competition. Therefore, waiting for bower desertion by other males may be the best bower acquisition tactic for males without bowers.     

Bower quality,number of decorations and mating success of male satin bowerbirds (Ptilonorhynchus violaceus): an experimental analysis

Bowerbirds build large bowers of twigs decorated with brightly coloured objects at display sites where males court females. The bower and its decorations are hypothesized to influence female choice in these birds. However, there have been no empirical tests of this hypothesis. Data from two years of field research on the satin bowerbird (Ptilonorhynchus violaceus) show: (1) an extremely skewed distribution of matings among males, and (2) a consistent pattern of female preference for particular males, especially those with well-constructed, highly-decorated bowers. These results support the hypothesis that bower quality is important in influencing female mating preferences. In particular, they support the ‘marker’ hypothesis, which suggests that the construction of bowers evolved to provide females with information about the relative quality of males.     

Vocal Mimicry of Alarm‐Associated Sounds by a Drongo Elicits Flee and Mobbing Responses from Other Species that Participate in Mixed‐Species Bird Flocks

A growing number of studies have shown that vocal mimicry appears to be adaptive for some bird species, although the exact function of this behaviour varies among species. Previous work has looked at the function of the vocal mimicry of non‐alarm sounds by the Greater Racket‐tailed Drongo (Dicurus paradiseus). But drongos also imitate sounds associated with danger, such as predators' vocalisations or the mobbing‐specific vocalisations of other prey species, raising the question of whether the function of mimicry can vary even within a species. In a playback experiment, we compared the effect on other species of different drongo vocalisations including: (1) predator mimicry, (2) mobbing mimicry, (3) drongo species‐specific alarms, (4) drongo species‐specific non‐alarms and (5) a control (barbet) sound. Both mobbing mimicry and drongo species‐specific alarms elicited flee responses from the most numerous species in the flocks, the Orange‐billed Babbler (Turdoides rufescens). Mobbing mimicry also elicited mobbing responses from the Orange‐billed Babbler and from another gregarious babbler, the Ashy‐headed Laughingthrush (Garrulax cinereifrons); when responses from both species were considered together, they were elicited at a significantly higher level by mobbing mimicry than by the barbet control, and a level that tended to be higher (0.07 < p < 0.10) than the response to drongo‐specific alarms. Predator mimicry elicited flee and mobbing responses at an intermediary level. Our results support the hypotheses that mobbing mimicry is a specific category of mimicry that helps attract the aid of heterospecifics during mobbing and that alarm mimicry can in some cases be beneficial to the caller.     

Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality

Much attention has been devoted to understanding the evolutionof elaborate male ornaments and how they may signal male quality.However, the evolution of multicomponent sexual signals remainspoorly understood, and past research on this type of signalinghas been largely theoretical. Satin bowerbirds, Ptilonorhynchusviolaceus, are polygynous, are sexually dichromatic, and constructsexually selected display structures (bowers): a model systemfor investigating the evolution and signal function of multiplesexual signals. We studied the interrelationship between bowerfeatures, plumage coloration, and indicators of male qualityin this species. To do this, we located the bowers of male satinbowerbirds in rainforest in Queensland, Australia, and quantifiedbower quality. We captured the male bower owners and used reflectancespectrometry to objectively measure the plumage coloration ofseveral body regions. We measured various indicators of malehealth and condition, including the intensity of infection fromectoparasites and blood parasites. Bower quality and male ultravioletplumage coloration were significantly correlated. By using multipleregression analyses, we show that bower quality predicts ectoparasiteload and body size, whereas ultraviolet plumage coloration predictsthe intensity of infection from blood parasites, feather growthrate, and body size. Our findings support the multiple messageshypothesis of multicomponent signals: Female satin bowerbirdsshould assess both male and bower features to choose the highestquality mates.     

Imitating the neighbours: vocal dialect matching in a mimic-model system

Vocal mimicry provides a unique system for investigating song learning and cultural evolution in birds. Male lyrebirds produce complex vocal displays that include extensive and accurate mimicry of many other bird species. We recorded and analysed the songs of the Albert's lyrebird (Menura alberti) and its most commonly imitated model species, the satin bowerbird (Ptilonorhynchus violaceus), at six sites in southeast Queensland, Australia. We show that each population of lyrebirds faithfully reproduces the song of the local population of bowerbirds. Within a population, lyrebirds show less variation in song structure than the available variation in the songs of the models. These results provide the first quantitative evidence for dialect matching in the songs of two species that have no direct ecological relationship.     

Bower decorations attract females but provoke other male spotted bowerbirds: bower owners resolve this trade-off

Elaborate secondary sexual traits offset the costs that they impose on their bearer by facilitating reproductive benefits, through increased success in intrasexual contests or increased attractiveness to choosy mates. Some traits enhance both strategies. Conversely, I show that spotted bowerbirds Chlamydera maculata may face a trade-off. The trait that best predicts their mating success, numbers of Solanum berries exhibited on a bower, also provokes increased intrasexual aggression in the form of bower destructions by neighbouring bower owners, which reduce the quality of the male's bower. At natural berry numbers, levels of mating success in the population are skewed, but levels of destruction do not vary with berry number. When berry numbers are artificially exaggerated, increased levels of destructions occur, but mating success does not increase. When offered excess berries, either to add to the bower or artificially placed on the bower, bower owners preferred to use numbers of berries related to the number that they displayed naturally. This decision is made without direct experience of the attendant changes in destruction or mating success. This indicates that bower owners may assess their own social standing in relation to their neighbours and modulate their display accordingly.     

Molecular information on bowerbird phylogeny and the evolution of exaggerated male characteristics

Mitochondrial DNA cytochrome b sequences of 849 base pairs are reported from eight species of Australian bowerbirds. These sequences are used with three from the literature (Edwards et al., 1991) to investigate bowerbird phylogeny using maximum parsimony and maximum likelihood methods. With respect to the three outgroup species, bowerbirds are shown to be monophyletic with high confidence using the bootstrap. The monogamous Ailuroedus crassirostris (which does not clear display courts) is indicated as the sister group to other bowerbirds. The maypole-builders (Amblyornis macgregoriae and Prionodura newtoniana) are significantly supported as a clade indicating a common origin for maypole type bowers, despite large differences in the design of these species' bowers. The avenue-builders (Sericulus chrysocephalus, Ptilonorhynchus violaceus, Chlamydera maculata and C. nuchalis) are also monophyletic. The pattern of divergence in avenue builders accords with the predictions of Gilliard's (1956, 1963) “transferral effect”. The transference hypothesis is not supported by evidence suggesting that the dull plumage of Scenopoeetes is an ancestral condition in bowerbirds. The use of sticks to build bowers could have had a single evolutionary origin and been secondarily lost in Scenopoeetes, or evolved independently in the avenue and maypole builders.     

Vocal mimicry by the Black-browed Reed Warbler Acrocephalus bistrigiceps: objective identification of mimetic sounds

Vocal mimicry by the Black-browed Reed Warbler Acrocephalus bistrigiceps was investigated. To identify mimicry objectively, we measured similarities between the sounds of models and those of Warblers by means of Principal Component Analysis (PCA) using a set of acoustic parameters. Of the sounds suspected of being mimicry according to visual inspection of sonagrams, only 57% were identifiable as mimicry according to PCA. Previous studies have not included quantitative criteria for assessing vocal mimicry, and our results suggest that judgements might not be reliable in the absence of objective criteria. Male Warblers incorporated the mimetic sounds into their songs, and each male mimicked 2–5 species. We found no evidence that females preferred males with large mimetic repertoires. This suggests that vocal mimicry has not evolved in response to selection by females in this species, although our analysis did not reveal entire mimetic repertoires in the Warbler songs.     

The Costs of Male Display and Delayed Plumage Maturation in the Satin Bowerbird (Ptilonorhynchus violaceus)

The costs associated with the evolution of male display traits has attracted much attention in regard to the type of traits that evolve and the timing of their expression. We investigate these costs by using testosterone implants to alter the development of male display traits in the satin bowerbird (Ptilonorhynchus violaceus). Testosterone implants advanced the development of adult display traits in males with juvenile plumage. We then measured the costs of early expression of these characters in treated males. Testosterone implants caused young males to (1) become more involved in behavior normally carried out by older males when visiting bowers, (2) build bowers, and (3) molt prematurely into an adult plumage. No difference was observed between the testosterone-treated birds and controls in return rate or condition the year following treatment, suggesting that the physical costs of display are not high. We found that males in adult plumage are tolerated less, and are not displayed to as frequently as juvenile plumage males at the bowers of established bower holders. The causes of delayed plumage maturation are most consistent with the facilitated-learning hypothesis. That is, early development of adult characteristics reduces the opportunity of young males to learn display behavior critical for later reproductive success.