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.     

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.     

Female Mate Preference for Males Having Long and Symmetric Fins in the Bower-holding Cichlid Cyathopharynx furcifer

Female mate preference in a bower-holding cichlid, Cyathopharynx furcifer, was studied in Lake Tanganyika. Most males held territories with crater-shaped bowers in sand, but some males held territories without bowers. Territories were distributed adjacently and females visited them to spawn. After engaging in circling behaviour with the male, a female deposited eggs in the bower. Soon after spawning, the female picked the eggs up into her mouth and brooded them in places away from male territories. Female mate choice appeared to follow three steps: 1) females visited only bower-holding male territories, and more frequently visited territories of males that performed courtship displays at a higher frequency and had longer pelvic fins; 2) females preferred to start circling with males having longer and more symmetrical pelvic fins; 3) females chose males with more symmetrical pelvic fins as their mates. Less than 7% of females that visited male territories spawned eggs in the bowers. In contrast to other bower-holding species, bower size did not correlate with male reproductive success in C. furcifer. Bowers may therefore be essential as spawning sites or may function as a species recognition character for females. Female choice may be dependent instead on males having long and symmetrical pelvic fins apparent during the circling behaviour carried out in the bowers.     

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.     

The multiple signals assessed by female satin bowerbirds: could they be used to narrow down females' choices of mates?

Female choice based on multiple male traits has been documented in many species but the functions of such multiple traits are still under debate. The satin bowerbird has a polygynous mating system in which males attract females to bowers for mating; females choose mates based on multiple aspects of males and their bowers. In this paper, we demonstrate that females use some cues to decide which males to examine closely and other cues to decide which males to mate with. Female visitation rates to bowers were significantly related to male size and the males' 'solitary' display rates, and, to a lesser extent, to the numbers of bower decorations. After controlling for female visitation rates, it was found that a male's mating success was significantly related to his size and the rate at which he 'painted' his bower with saliva and chewed up plant material.     

SEQUENTIAL FEMALE ASSESSMENT DRIVES COMPLEX SEXUAL SELECTION ON BOWER SHAPE IN A CICHLID FISH

In many animals, sexual selection on male traits results from female mate choice decisions made during a sequence of courtship behaviors. We use a bower‐building cichlid fish, Nyassachromis cf. microcephalus, to show how applying standard selection analysis to data on sequential female assessment provides new insights into sexual selection by mate choice. We first show that the cumulative selection differentials confirm previous results suggesting female choice favors males holding large volcano‐shaped sand bowers. The sequential assessment analysis reveals these cumulative differentials are the result of selection acting on different bower dimensions during the courtship sequence; females choose to follow males courting from tall bowers, but choose to engage in premating circling with males holding bowers with large diameter platforms. The approach we present extends standard selection analysis by partitioning the variances of increasingly accurate estimates of male reproductive fitness and is applicable to systems in which sequential female assessment drives sexual selection on male traits.     

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.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

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.     

Bowers of the Great Bowerbird (Chlamydera nuchalis) remained unburned after fire: is this an adaptation to fire?

Fire plays an important role in the evolution of life-history characteristics of organisms living in fire-prone regions. Although there are many reports of plants exhibiting adaptations to reduce the harmful or lethal effects of fire, little is known about fire-resistance mechanisms among animals, other than fleeing responses. Here, we report observations that may represent a type of fire adaptation in a bird species: bowers in one population of the Great Bowerbird Chlamydera nuchalis remained unburned after fire. If a bower is destroyed by fire or other mechanisms during courtship and breeding season, the male may lose the opportunity to mate with females, thereby reducing his apparent fitness. Therefore, traits that minimise the damage to bowers from fires may be beneficial. By measuring the unburned areas surrounding bowers after fires, we showed that the survival of bowers after fires is unlikely to be solely related to chance. Our observations are consistent with the hypothesis that bower resistance to fire is an adaptation of the Great Bowerbird. However, it is also possible that unburned bowers are by-products of sexual selection.     

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.     

Vocal mimicry in spotted bowerbirds is associated with an alarming context

Although the presence of vocal mimicry in songbirds is well documented, the function of such impressive copying is poorly understood. One explanation for mimicry in species that predominantly mimic alarm calls and predator vocal isations is that these birds use mimicry to confuse or deter potential threats or intruders, so these vocalisations should therefore be produced when the mimic is alarmed and be uncommon in other contexts. Male bowerbirds construct bowers to display to females and anecdotal reports from the Ptilonorhynchus genus suggest that males mimic alarm sounds when disturbed at their bowers. We quantified and compared the rate of mimicry during disturbance to the bower by a human and in naturally occurring social contexts in a population of spotted bowerbirds Ptilonorhynchus maculatus. Male bowerbirds produced mimicry more than thirty times more frequently in response to bower disturbance than they did in any other context. Neither conspecifics nor heterospecifics were attracted to the bower area by mimicry. These data are consistent with the hypothesis that the production of mimicry is associated with a response to an alarming situation. Additionally, the predominance of alarm mimicry by spotted bowerbirds raises the possibility that the birds learn these sounds when they experience alarming situations and they reproduce them in subsequent alarming situations.     

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.     

Mating strategies in two species of dart-poison frogs: a comparative study

Comparative field studies of species of dart-poison frogs in the genus Dendrobates were carried out to test predictions from two hypotheses that attempt to explain female-female competition for mates in species of Dendrobates with male parental care. The sex role reversal hypothesis proposes that males invest so much time and energy in parental care that receptive males are rare relative to receptive females, and females compete to find and mate with receptive males. The parental quality hypothesis proposes that females compete to monopolize the parental effort of particular males, because they potentially suffer a cost when their mates care for the offspring of other females. Comparisons between species with male parental care (Dendrobates leucomelas) and female parental care (Dendrobates histrionicus) contradicted prediction of the sex role reversal hypothesis, but were consistent with predictions of the parental quality hypothesis. Male D. histrionicus did not compete for mates more aggressively than male D. leucomelas, and male D. leucomelas were not more selective about mating than male D. histrionicus. Female D. leucomelas and D. histrionicus were both selective about mating; female D. leucomelas associated with and competed for particular males, whereas female D. histrionicus did not.     

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.     

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.     

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.      

Co-option of male courtship signals from aggressive display in bowerbirds

The pre-existing trait hypothesis suggests that females evolve a mating preference for an already existing male trait. This hypothesis poses a simple resolution to Darwin's long-standing question of how elaborate, male display traits evolve. The frequently observed convergence of aggressive and courtship displays across a wide array of species provides the only current support for this hypothesis. Here we provide much more detailed supporting evidence from bowerbird skrraa calls used in aggression and courtship. Consistent with the pre-existing trait hypothesis we show that (i) putatively co-opted skrraa calls used in courtship and aggression are homologous, (ii) skrraa calls were used in aggression in bowerbirds before being used in courtship, (iii) historically, intense, aggressive-like courtship calls were present near the time of co-option, and (iv) bower types contemporaneous with co-option emphasize design features that provide females protection from the adverse effects of intense courtship displays. These results, plus evidence for a female preference for males with intense aggressive-like courtship skrraa calls, suggest that aggressive skrraa calls have been co-opted for use in male courtship display     

On the function of female ornaments: male bluethroats prefer colourful females

Female ornaments in animals with conventional sex roles have traditionally been considered non-functional, being merely a genetically correlated response to selection for male ornamentation. Alternatively, female ornaments may be influenced by selection acting directly on the females, either through female–female competition or male choice. We tested the latter hypothesis in mate choice experiments with bluethroats (Luscinia s. svecica), a passerine bird in which females vary considerably in coloration of an ornamental throat patch. In outdoor aviaries placed in prime breeding habitat, males were allowed to choose between a colourful and a drab female. We found that males associated more with, and performed more sexual behaviours towards, colourful females. Female coloration was not age-related, but correlated significantly with body mass and tarsus length. Thus, we have demonstrated both a male preference for female ornamentation, and a relationship between ornament expression and female body size, which may be indicative of quality. Our results refute the correlated response hypothesis and support the hypothesis that female ornamentation is sexually selected.     

Sexual swelling in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis

Various hypotheses have been proposed to account for the functionof sexual swellings in female primates, but few empirical dataexist to test predictions arising from these hypotheses. Controversyhas recently arisen over a field study that appeared to supportthe predictions of the reliable indicator hypothesis. This hypothesisproposes that females compete for males or matings, that differencesin swelling size between females reliably advertise female quality,and that males use swelling characteristics to differentiallyallocate mating effort to females with certain swelling characteristics,hence to females of higher quality. To provide an independenttest of this hypothesis, we collected data concerning the sizeand coloration of 40 sexual swellings for 29 semi-free-rangingfemale mandrills, varying in age and parity, along with dataconcerning the behavior of males toward the females, and comparedthese with the long-term reproductive history of the females.We examined the following predictions: (1) swelling characteristicsare consistent across subsequent cycles for individual females,(2) swelling characteristics indicate aspects of female reproductivequality, and (3) males prefer to mate with females that showparticular swelling characteristics. Our results support prediction1; we found little change in swelling characteristics acrossswellings for individual females. However, we found no significantrelationships between female reproductive history and swellingcharacteristics and, thus, no support for prediction 2. Finally,we found only limited support for prediction 3; females withlarger (wider) sexual swellings were more likely to have a spermplug when maximally swollen. However, male mate-guarding wasnot significantly related to female swelling characteristics.Furthermore, in situations in which more than one female wasmaximally swollen, the alpha male (who has "free" choice) didnot show the most interest in the female with the largest swelling.We conclude that the reliable indicator hypothesis does notexplain variation in sexual swellings in female mandrills.