Cooperative courtship display in Long-tailed Manakins Chiroxiphia linearis: predictors of courtship success revealed through full characterization of display

Abstract

The Pipridae comprise 52 species of manakins with a wide variety of courtship behaviours, ranging from solitary display, to traditional leks, to cooperative display. Long-tailed Manakins (Chiroxiphia linearis) exhibit an exploded lek-breeding system wherein two unrelated males cooperate to perform complex courtship displays for females. Our objectives in this study were to fully characterize the courtship display of Long-tailed Manakins, to evaluate the sequence and stereotypy of the display, and to investigate specific predictors of copulation success. Whereas the display of Long-tailed Manakins has traditionally been divided into two major parts, the hopping display and the butterfly display, we identified and characterized 16 individual display elements within these larger components of the display. We also determined that some aspects of the display are highly structured and stereotypical in performance, such that certain elements of the display are highly likely to be preceded or followed by particular elements. Nevertheless, other aspects of the display were much more flexible in terms of element sequence. We also found that the length and rate of performance of individual display elements were highly variable across displays. We therefore evaluated whether individual elements of the display could predict courtship success. Our results show that a number of highly correlated elements, namely upright postures, bounces, angel flights, and bows, can predict whether a display ends in copulation with a female. This research enhances our understanding of male display behaviour and female choice in Long-tailed Manakins, and may shed some light on the evolution of complex courtship displays in birds.

Zusammenfassung

Gemeinschaftliches Balzen bei Langschwanzpipras ( Chiroxiphia linearis ): eine vollständige Beschreibung des Balzverhaltens bietet Prädiktoren für ein erfolgreiches Werben

Die Familie der Pipras (oder auch Manakins) umfasst 52 Arten mit einem weiten Spektrum unterschiedlichen Balzverhaltens: es gibt einzeln balzende Tiere, Balz an bekannten Balzplätzen und auch gemeinschaftliches Balzverhalten. Die Langschwanzpipras (Chiroxiphia linearis) zeigen ein detailreiches Balz-und-Brut-System, in dem zwei nicht verwandte Männchen bei der Werbung um Weibchen zusammenarbeiten und dabei sehr komplexe Verhaltensweisen zeigen. Ziel unserer Untersuchung war es, das Balzverhalten der Langschwanzpipras komplett und im Detail zu erfassen und zu beschreiben, Wiederholungen und Stereotypen von Verhaltenselementen zu bewerten und zu untersuchen, ob es spezifische Prädiktoren für erfolgreiche Kopulationen gibt. Traditionell unterteilt man das Balzverhalten der Langschwanzpipras in zwei Hauptabschnitte: einen Hüpf- und einen Schmetterlings-Teil; wir identifizierten und beschreiben innerhalb dieser großen Verhaltenskomponenten 16 einzelne Verhaltenselemente und stellten darüber hinaus fest, dass einige Abschnitte dieser Verhaltensweisen hoch strukturiert sind, ständig wiederholt werden und mit hoher Wahrscheinlichkeit auf ganz bestimmte andere Verhaltenselemente folgen, bzw. dass sie ganz bestimmten Elemente vorangehen. Es gab andere, in ihren Reihenfolgen deutlich flexiblere Verhaltenselemente, und wir fanden weiterhin, dass Dauer und Häufigkeit einzelner Verhaltenselemente innerhalb des gesamten Balzverhaltens sehr variabel waren. Deshalb untersuchten wir, ob einzelne dieser Elemente einen Balzerfolg vorhersagen ließen. Unsere Ergebnisse zeigen, dass eine ganze Reihe miteinander hoch korrelierter Elemente - in erster Linie das Aufrichten, Hüpfen, Verbeugen und der „Engelflug“- Vorhersagen zulassen, ob die Balz zu einer Kopulation mit einem Weibchen führt. Diese Ergebnisse vertiefen unser Verständnis vom männlichen Imponierverhalten und der weiblichen Partnerwahl bei Langschwanzpipras und bringen vielleicht etwas mehr Licht in die Evolution des sehr komplexen Balzverhaltens von Vögeln.

Introduction

Sexual selection has led to the evolution of extreme forms of courtship in some species, from exaggerated physical traits to elaborate displays (Darwin 1859). This is especially evident in polygynous species, where males are emancipated from parental duties and subject to enhanced female choosiness (Trivers 1972; Emlen and Oring 1977). In lekking species, males gather at communal lekking arenas to perform courtship displays for females; females evaluate these displays, as well as exaggerated physical characteristics of males, to choose a mate (Bradbury and Gibson 1983; Kirkpatrick and Ryan 1991). Lekking species typically exhibit very high reproductive skew with only one or few males at a display site obtaining all mating opportunities (Kirkpatrick and Ryan 1991).

Manakins (family Pipridae) comprise 52 species of suboscine passerine birds distributed throughout Central and South America (Snow 2004; McKay et al. 2010; Ohlson et al. 2013). Many species of manakins exhibit lek-breeding behaviours and are known for their elaborate courtship displays, but a great deal of variation exists among species (Snow 2004; Prum 2010). Within the genus Chiroxiphia, two or more males usually perform joint cooperative displays at leks, or display areas, to attract females. In Long-tailed Manakins, C. linearis, for example, two unrelated males coordinate their efforts to perform elaborate dual-male displays that include vocalizations, visual traits, and behaviours to attract and entice females to mate (Slud 1957; Foster 1977; McDonald 1989a, b; McDonald and Potts 1994). Unlike other manakin species, the coordination of two males is obligate in this system to successfully attract females for copulations (Foster 1977). In addition, males undergo delayed plumage maturation whereby they develop a distinct pre-definitive plumage pattern for each of the first 4 years after hatch, finally attaining the definitive adult plumage in their fifth year (Doucet et al. 2007). Three to thirteen males are affiliated with each lekking arena, or display area, including an alpha and beta pair, several other subordinate definitive males, as well as a mixture of younger males in pre-definitive plumage (Foster 1977; McDonald 1989b, 2007; Trainer et al. 2002). All males affiliated with a display area can perform displays in the absence of females; however, only the alpha and beta male perform the courtship display for females, and only alpha males copulate with females (McDonald 1989b).

The coordinated display of C. linearis consists of both acoustic and visual display elements. Pairs of alpha and beta males produce toledo duet vocalizations to attract females to their display area where they then perform a coordinated display comprising two main components: the hopping display and the butterfly display (Foster 1977; McDonald 1989b). These displays are first performed jointly by the alpha and beta male, and eventually lead to a solo performance of the butterfly display by the alpha male. The solo display consists of the same display elements present in dual displays except for elements that require the participation of both males. Previous research has shown that the mean output of toledos was correlated with female visitation, and that the length of the butterfly display was correlated with reproductive success (i.e. the number of displays that ended in copulation; McDonald 1989b); however, many individual subcomponents of the display could influence this relationship. For example, as the length of the butterfly display increases, so does the potential number of additional elements included in the display. By characterizing the full display in detail, we may be able to determine whether unique display elements can influence male mating success.

Although a considerable amount of research has been conducted on the breeding biology, behaviour, plumage, and vocalizations of Long-tailed Manakins (Foster 1976, 1977; McDonald 1989b; Trainer and McDonald 1993; Doucet et al. 2007), the individual elements of the courtship display have not yet been described in full detail. Here, we characterize and quantify 16 unique visual elements of the Long-tailed Manakin courtship display. To determine whether elements of the display follow a stereotypical pattern, we provide a generalized sequence of courtship behaviour using transitional probability matrices. We then examine whether the performance of individual display elements can predict copulation success.

Methods

We conducted our research in the Área de Conservación Guanacaste, sector Santa Rosa, a UNESCO World Heritage Site in northwestern Costa Rica. Our long-term study population is located in a small area of evergreen forest (approximately 2 km2) surrounded by tropical dry forest. With annual capture and banding efforts, over 700 manakins have been fitted with unique colour bands over the past 9 years.

Long-tailed Manakins are a Neotropical suboscine species with a distribution that ranges from Costa Rica to Mexico. Like many other manakins, they exhibit sexual dichromatism, a frugivorous diet, a lack of male parental care, and a lek-based mating system (Foster 1976, 1977; McDonald 1989b). Unlike several other Piprid species, Long-tailed Manakins do not produce mechanical noises with their feathers. Their 4-year delay in plumage maturation is longer than most other manakins (Doucet et al. 2007), for which a 1- to 2-year delay is common (Snow and Lill 1974; Snow 2004), and allows for easy identification of pre-definitive age in the field. The majority of the courtship display takes place on or around a primary display perch located within each display area. Males use horizontal vines as display perches, and each display area contains one primary display perch and up to four additional secondary perches, with an average of 1.75 ± 0.17 perches at display areas with recorded dances for females. Displays for females usually take place on the primary display perch unless there is a disturbance at that perch, but subordinate males occasionally use additional perches to perform the display in the absence of females. Secondary perches within a display area are located within a maximum of 36 m from each other (Ward 2012).

From 2010 to 2012, we located and mapped the GPS coordinates of manakin display perches and assigned each of them to discrete display areas based on the attending alpha males. Throughout the breeding seasons, we targeted 39 active display areas and set up video cameras within 5–15 m of display perches and recorded behavioural data for approximately 5 h starting at dawn. We targeted active display areas including both primary and secondary display perches. We sampled active display areas a minimum of 3–5 times per season for a total of approximately 2,500 h of video footage. In addition, we conducted over 100 h of live observations in the field in 2-h segments at display areas and recorded our observations using a hand-held voice recorder.

We identified and described 16 individually distinct elements of the courtship display based on observations in the field and from video footage. We considered elements to be unique if each posture or behaviour was always executed in a similar manner across males and display areas, if behaviours were never executed partially (unless disrupted by conspecifics or heterospecifics), and if they were independent of other discrete behaviours that immediately preceded or followed them. Elements could be repeated, and did not necessarily need to be interspersed with other elements. We scored videos for each of these individual behavioural elements in terms of frequency of occurrence, duration, or presence/absence during courtship displays. We also scored videos for dominance behaviours, copulations, and vocalizations.

Male Long-tailed Manakins exhibit both dual and solo display courtship behaviour, and a courtship display may include either solo or dual display, or both. A courtship display refers to one continuous display (i.e. no more than 1 min between performed elements) as performed by a single alpha male, a pair of definitive males, or a combination of solo and dual displays for a female. Males often flew between perches surrounding the main display perch, thus leaving the frame of our videos. A maximum of a 1-min waiting period ensured that males had in fact ceased displaying, as opposed to performing part of the display outside the frame. Courtship displays may include any elements of the display, but do not necessary include all display elements, and a single courtship display may include multiple solo and dual displays. A bout of hopping or butterfly display refers to only those segments of the display.

Statistical analysis

We were interested in fully characterizing the courtship display elements performed by Long-tailed Manakins. We scored videos for the length of courtship displays and the frequency of occurrence of each display element. We combined individual elements into larger categories of display to quantify durations for those larger categories and to calculate display rates for some of the individual display elements; all descriptive statistics are reported as mean ± SE (JMP 10.0). Female behaviour during male display data were collected during 2010–2011 only and are reported as rates per minute of male display.

To determine the sequence and stereotypical nature of the display, we scored videos of courtship behaviour for sequences of specific display elements, based on the frequency of occurrence of each display element, using JWatcher+video software (v.1.0; Blumstein and Daniel 2007). We created transitional probability matrices based on all courtship displays performed in the presence of females, as well as matrices based on successful courtship displays only (i.e. those that ended in copulation). First-order transitional probability matrices demonstrate the probability that one display element follows another. First, we created a matrix that included repeated events (e.g. a butterfly flight followed by another butterfly flight), to illustrate the degree to which certain elements tended to repeat themselves within a display. Next, we recalculated the matrix so that repeated events were not incorporated and we could more accurately portray the progression from one element to the next. Using these matrices, we created a schematic of the display to represent the sequence of elements as they most commonly occur (more than 10 % of the time) during dances for females, by linking elements with high transition probabilities. We performed these sequence analyses on a subset of displays for females, totalling 43 courtship displays from 22 different display areas. To investigate whether the pattern of display behaviour differed during successful displays, we also created a schematic based on 18 courtship displays ending in copulations. To investigate the structure of the display at a higher order, we also created second-order transitional probability matrices using all courtship displays for females (including those that did and did not end in copulation). These matrices illustrated the likelihood that given two specific elements occurred in a certain order, a third element followed. This analysis is useful for determining if certain behavioural events can predict other behaviours (i.e. if combinations of display elements predict other display elements), or if behaviours are equally probable and independent of each other.

Previous studies have revealed that the length of butterfly display is correlated with copulation success (McDonald 1989b; Ward 2012); however, we were interested in looking at individual elements within the display to determine which particular elements may be influencing courtship success. To determine which specific elements of the courtship display predict courtship success in Long-tailed Manakins, we measured the total length of displays or rate of occurrence of display elements per minute of display, and performed generalized linear mixed models in IBM SPSS Statistics (20.0). We fitted our models with binomial distributions (logit-linked functions) and performed binary logistic regressions. Individually, we included each of 14 display elements as fixed factors to investigate whether the performance of one or more of these elements could predict a successful courtship display. A few display elements were not quantified (only scored for presence), or had small sample sizes, and were therefore omitted from these analyses. To account for repeated measures of individuals, we classified the display area as a random factor in our analyses. Since alpha and beta males have high lek fidelity, using display area as a random factor controls for repeated sampling of alpha–beta pairs. We performed these regressions on all courtship displays for females, including those that ended in copulation (i.e. may include solo displays, dual displays, or both). To assess variability in the performance of individual display elements, we calculated coefficients of variation for each display element. We also performed Spearman’s rank correlations on the display variables of interest to determine the level of intercorrelation between elements.

Results

Courtship display

We identified 16 unique visual elements performed by Long-tailed Manakins during courtship displays. All elements were performed in the presence of a female, though some elements were performed more rarely than others, and not all were necessary to elicit copulation. Manakins also produced 14 vocalizations; only those associated with specific elements of the display are mentioned here (see Trainer and McDonald 1993 for full description of vocalizations).

The alpha male begins by singing teeamoo calls which function to attract a beta partner to the display area (Trainer and McDonald 1993). This call is generally given in the lower canopy above the display perch. Once the beta arrives, the alpha and beta begin a series of simultaneous toledo calls from the canopy to attract females to the area (McDonald 1989a, b). When a female arrives, the males descend to the display perch and begin their elaborate courtship display which consists of at least 16 individual dance elements.

The visual components of the courtship display can be classified into two main categories based on the types of physical manoeuvres involved: the hopping display and the butterfly display, both of which have been previously described (Slud 1957; Foster 1977; McDonald 1989b), with three additional elements (buzz-weent, lightning bolt, and angel flight) identified by McDonald (2010). However, within these two categories are a number of individual elements that we characterize here for the first time. For previously described displays, we maintain the terminology established by Slud (1957), Foster (1977), and McDonald (1989a, 2010). For newly described elements, we use terminology that reflects any similarities to previously described display elements of other manakin species whenever possible. Our descriptions and descriptive statistics are based on 98 courtship displays (consisting of 82 dual displays and 56 solo displays) performed by definitive males for females at 21 display areas. Rates are reported based on the length of time spent performing each type of display (e.g. leapfrog rate is based on the time spent performing the hopping portion of the display, and butterfly flight rates are based on the total time spent performing the butterfly portion of the display).

Hopping display

Stationary display Two males perch roughly 10–15 cm apart on the display perch. To initiate the first part of the dual display, one male crouches down in a bowing position with his head lowered and his rump and tail in the air then proceeds to vibrate his body (Fig. 1a). While in this position, the male often appears to run in place, alternately lifting his feet. This display appears to occur in anticipation of the hopping elements of the display (see popcorn hops and leapfrogs, below), similar to the stationary display in Band-tailed Manakins (Pipra fasciicauda) and the wing shiver display in Crimson-hooded Manakins (Pipra aureola; Snow 1963a, b; Robbins 1983). This display was recorded as present or absent and was common, preceding 78 % of hopping bouts.

Fig. 1
figure1

Elements of the Long-tailed Manakin Chiroxiphia linearis courtship display: a two males performing leapfrogs, with lower male performing stationary display; b male exhibiting buzz-weent display on primary display perch (shaded), followed by a set of tucked wing flicks on a perch below; c male performing butterfly flight towards perch, followed by a bounce upon landing; d arrow depicting flight pattern of s-shaped dart, followed by an about face upon landing; e male exhibiting bill wipes; f male exhibiting back-and-forth displays; g arrow depicting flight pattern of lightning bolt, followed by an upright posture upon landing; h male performing frenzied flutter; i male performing an angel flight and landing in a bow position (Illustrations by K.C. Lukianchuk)

Popcorn hop After initiating with the stationary display, the same male leaps into the air above the display perch and appears to hover there for several moments by rapidly flapping his wings. While in the air, the manakin hunches his back, lowers his head, and stretches his legs straight down, apparently drawing attention to his blue mantle, red crown, and orange legs. He then descends to the display perch in the same location where he began. As the first male lands, the second follows by hopping into the air in the same fashion as the first. The two males alternate this process. While the male on the display perch waits for his partner to descend, he often performs the stationary display until it is his turn to jump. Similar display elements are exhibited in Lance-tailed (C. lanceolata; up-and-down display; DuVal 2007) and Orange-crested Manakins Heterocercus aurantiivertex (vertical dancing jumps; Alonso 2000). The popcorn hop was previously described by Slud (1957), and later Foster (1977) and McDonald (1989a).

Leapfrog Similar to popcorn hops, males alternate hopping into the air; however, instead of landing in the same place where he begins, the hopping male leaps backwards over his dance partner and take his place on the display perch. Meanwhile, instead of exhibiting the stationary display, the male on the display perch runs forward (towards the female) to take the place of the first male (Fig. 1a; Online Resource 1). The act appears as a backwards leapfrog dance and changes orientation depending on which side of the display perch the female is observing from. This type of display is common among other Chiroxiphia species (Gilliard 1959; Snow 1971; Foster 1977; DuVal 2007). Males frequently alternate between leapfrogs and popcorn hops within the same hopping display. On average, hopping bouts lasted for 36.6 ± 3.08 s with an average rate of 58.4 ± 1.6 hops/leapfrogs per minute of hopping display, (20.7 ± 2.0 hops/min and 38.7. ± 2.39 leapfrogs/min) with a single hop or leapfrog defined as the action of one individual male hopping or leaping over the other. The leapfrog was previously described by Slud (1957), Foster (1977) and McDonald (1989a).

While males participate in popcorn and leapfrog hops they emit calls that are synchronized with each hop. These calls have been described phonetically as nyanyownh (Trainer and McDonald 1993). Males appear to switch between hops and leapfrogs depending on the location of a female (i.e. males often use leapfrogs when female is on the display perch, and hops when the female is on a nearby perch; per. obs.).

Buzz-weent As the leapfrog display progresses and becomes more intense, males quicken their paces and reduce the heights of their hops, until the nyanyownh calls degenerate into a noisy series of buzzes. Eventually, the alpha male gives a sharp weent call at the peak of his last hop and descends quickly in an arc down past the display perch and swoops up to land on a nearby perch (Fig. 1b; Online Resource 1; McDonald 1989a, b). The beta remains on the display perch in a crouched position while the alpha completes this display. This call and accompanying manoeuvre is only exhibited by the dominant male of the pair, and is often absent when younger males are displaying in the absence of females. After the alpha performs a buzz-weent, the beta either remains on the display perch until the alpha begins the butterfly portion of the dual display, starts the butterfly dual display himself, or he leaves, allowing the alpha to begin his solo dance. Homologues to the buzz-weent display can also be seen in other Chiroxiphia manakins (Foster 1981; DuVal 2007). Approximately 10 % of hopping bouts ended in buzz-weents, with up to six per courtship display.

Tucked wing-flick Once the alpha performs a buzz-weent and lands on a nearby branch (either a horizontal or vertical branch), he begins to repeatedly and very rapidly flick his wings back behind his body without spreading them so that they almost meet at the back (Fig. 1b, lower panel). Males performed an average of 8.5 ± 1.8 wing flicks per minute of hopping display, before moving on to the butterfly display (tucked wing flicks often occurred off camera, and therefore this rate is based on only the five displays in which it was observed). Other manakins exhibit excitement and display behaviours that involve a more subtle wing-flicking motion (Foster 1981; Prum 1985, 2010; Tello 2001; Rosselli et al. 2002; Shorey 2002; Durães 2009); however, this particular display in Long-tailed Manakins is very pronounced and occurs only directly after a buzz-weent, suggesting it is a unique display behaviour rather than a general excitement behaviour that occurs throughout the display.

Butterfly display

All elements of the butterfly display were observed in both dual and solo male performances. Although males performed most elements to some degree at each display area, some elements that were consistently performed at some display areas were not observed at others. Males exhibited two categories of elements during the butterfly display, including flight elements and landing postures. The average length of individual bouts of butterfly display (including any display elements present) was 22.2 ± 1.73 s for dual male displays, and 190.3 ± 53.81 s for solo displays. Although copulations are not considered an element of the display, we include their description at the end of this section as they only occur directly after the butterfly display.

Butterfly flight Males make short, slow flights between the display perch and other nearby perches with laboured wing flaps that resemble those of butterflies in flight (Fig. 1c; Online Resource 1). This is the iconic element for which the butterfly display was named and was previously described by Slud (1957) and McDonald (1989b). Butterfly-like flights are also seen in Blue-crowned (Lepidothrix coronata), Band-tailed, White-throated (Corapipo gutturalis), White-ruffed (Corapipo leucorrhoa), and White-crowned Manakins (Pipra pipra); however, there are variations among postures, as seen in the vertical body positions of White-ruffed Manakins during flights (Snow 1960; Robbins 1983; Théry 1990; Rosselli et al. 2002; Castro-Astor et al. 2007; Durães 2009). Butterfly flights are the most common element in the butterfly display, with an average of 27.7 ± 1.8 flights/min of dual butterfly display, and 19.1 ± 2.2 flights/min of solo display.

Dart Darts are short flights between the display perch and other nearby perches; each flight occurs very rapidly, with minimal wing flaps between take off and landing. They appear almost torpedo-like as males dart between perches. This display often alternates with butterfly flights. McDonald (2010) mentioned the presence of ‘rapid landings’ during solo displays; however, males do perform darts during dual displays as well. Occasionally males fly in an ‘s’-shaped flight pattern or a rapid upward arc towards the display perch (Fig. 1d). Straight rapid flights are also seen in the White-ruffed Manakin (Rosselli et al. 2002), and flights with s-curved swoops are exhibited by Crimson-hooded Manakins and Golden-headed Manakins (Pipra erythrocephala; Prum 1990). Males exhibited an average of 6.27 ± 1.34 darts/min of dual butterfly display, and 2.47 ± 0.83 darts/min of solo butterfly display.

Bounce A male lands briefly on the perch and then immediately takes flight back in the direction from which he came, appearing to bounce off the perch (Fig. 1c, Online Resource 1, also seen in the Lance-tailed Manakin; DuVal 2007). Males performed an average of 0.14 ± 0.06 bounces/min of dual butterfly display and 0.53 ± 0.13 bounces/min of solo butterfly display.

Bill wipe Males are often seen wiping their bills against the display perch between butterfly flights and darts, in place of bounces, upright postures, or bows (Fig. 1e). Males exhibited an average of 1.19 ± 0.11 bill wipes/min of dual butterfly display and 1.22 ± 0.21 bill wipes/min of solo butterfly display.

Upright posture A male lands on the perch after performing a flight element and proceeds to stretch his body, head, and bill upwards, before taking off again (Fig. 1g; Online Resource). This is similar to the upright postures seen in Red-headed (Pipra rubrocapilla) and Round-tailed Manakins (Pipra chloromeros; Tello 2001; Castro-Astor et al. 2004). Males performed an average of 2.50 ± 0.30 upright postures/min of dual butterfly display and 2.51 ± 0.38 upright postures/min of solo butterfly display.

About face A male lands on a perch after a flight element, then quickly performs a 180° turn on the perch. This quick turn is either done in place, or results in the male landing approximately 10–15 cm further down the length of the perch, and appears almost as if he slides across the perch while switching directions (Fig. 1d; Online Resource 1). We did not quantify about faces, but we included them in our analyses of display sequence and stereotypy. About faces are seen in other manakins including the Golden-headed, Lance-tailed (quick-turn), White-throated, White-crowned, and Round-tailed Manakins (Théry 1990; Tello 2001; Castro-Astor et al. 2004, 2007; DuVal 2007).

Lightning bolt Between butterfly flights and darts, males occasionally fly to higher branches in the canopy to perform this display, in which they abruptly drop from the sky in a rapid vertical (or slightly diagonal) descent to land on the display perch directly below (Fig. 1g, McDonald 2010). Members of the genus Corapipo exhibit an above-the-canopy flight display, which incorporates a rapid plummet downwards from the canopy; however, it also includes a rapid upwards flight accompanied by a buzzy vocalization (Prum 2010), which is not seen in Long-tailed Manakins. Males performed lightning bolts fairly infrequently, at an average of 0.26 ± 0.06 lightning bolts/min of dual butterfly display and 0.14 ± 0.05 lightning bolts/min of solo butterfly display.

Back-and-forth During bouts of the butterfly display, one male often darts rapidly from side to side (approximately 10–15 cm) on a horizontal (or more rarely, vertical) branch, seemingly using one wing at a time to propel himself in the opposite direction (Fig. 1f; Online Resource 1). Males perform this display either individually or as a dual display (with two males facing each other on separate branches). This display is similar to the back-and-forth display of the Lance-tailed Manakin, the side-to-side display of the Band-tailed Manakin, and the side-to-side slide in both the Red-headed Manakin and the Round-tailed Manakin (Robbins 1983; Tello 2001; Castro-Astor et al. 2004; DuVal 2007). Males performed an average of 2.67 ± 1.02 back-and-forths/min of dual butterfly display and 1.24 ± 0.69 back-and-forths/min of solo butterfly display.

Angel flight While on the perch, the male does a short, arcing, vertical flight and lands approximately 10–15 cm further down the perch, with his wing flaps exaggerated so the wings touch at each flap (Fig. 1i; Online Resource 1; McDonald 2010). Angel flights can also be performed from another perch towards the primary display perch. Usually the alpha male performs this display so that he positions himself directly next to the female prior to copulation. However, the alpha and beta occasionally perform this flight during the dual-male butterfly display, especially when multiple females are present or during displays in the absence of a female (pers. obs.). Males performed an average of 0.07 ± 0.03 angel flights/min of dual male butterfly display and 0.21 ± 0.04 angel flights/min of solo butterfly display.

Bows After the alpha male performs an angel flight towards a female, he assumes an exaggerated bowing posture with his crest erected and spread, and his head lowered towards the front of the female (Fig. 1i, Online Resource 1). Immediately after this display the alpha male makes a copulation attempt. On occasion males perform this display between flight elements during dances in the absence of females. Males performed an average of 0.04 ± 0.02 bows/min of dual male butterfly display and 0.21 ± 0.04 bows/min of solo butterfly display.

Copulation Females observing the display typically leave the display area without copulating, and can leave at any time throughout the courtship display. However, if a female remains for the entire display and is willing to copulate, she settles on the main display perch and allows the alpha male to mount her immediately following his angel flight and bow displays (Online Resource 1). After a short copulation, the male leaves the display area and the female generally remains on the display perch for a few seconds up to a few minutes and preens. Copulations are not considered an element of the display, but rather the result of a successful display. Only 16 % of 99 displays for females included a copulation event. Females generally copulated with males only once per display; however, 31 % of displays that contained copulations included two copulation events. We were unable to determine whether multiple copulation events within a single display involved the same female.

Female display

Some females are actively involved in the courtship display and two of the manoeuvres they exhibit, jumps and back-and-forths, appear to indicate excitement as they increase with display length and may indicate a female’s likelihood of copulating (Ward 2012). Hatch-year males tend to resemble females in plumage; however, female behaviour is distinct from that of male courtship behaviour, and is described below.

Jump Females often exhibit small jumps in place while observing courtship displays (1.05 ± 0.20 female jumps per minute of male display).

Perch change Females often observe the courtship display directly from the main display perch; however, they also fly to nearby branches and back, as if to observe the display from other angles (1.36 ± 0.20 female perch changes per minute of male display).

Angel flight On occasion, females fly between perches performing flights that appear to be identical to angel flights displayed by males. This usually occurs during an intense bout of the solo butterfly display, in which the female rapidly follows the alpha male from branch to branch. Females can also perform angel flights on a single perch, ascending and descending a short distance down the same perch.

Back-and-forth This display is identical to the back-and-forth display performed by males, and is also exhibited by female Lance-tailed Manakins (DuVal 2007). Females exhibited 5.40 ± 1.26 back-and-forths per minute of male display.

Post-copulatory position Immediately following copulation, females remain on the display perch and slowly stretch their legs so their bodies extend upwards for a few seconds.

Dancing in the absence of females

Pre-definitive males tend to associate with several display areas and interact with many males before they gradually become associated with a primary display area (McDonald 2007). Males of all ages were often seen displaying in the absence of females, and there were several notable differences between these displays and displays for females. Anywhere from one male up to five or six males displayed simultaneously, with any combination of age groups participating. The exact function of these displays is not known, though it is likely that they serve as a form of practice for younger males (as observed in other species of manakin; Snow and Snow 1985; McDonald 2007; Durães et al. 2008; Schlinger et al. 2008; Durães 2009; Coccon et al. 2012), and they may also help establish dominance relationships among males.

Frenzied flutter This display appears to be a pseudocopulation, in which males flutter on the display perch in the same fashion as if they had mounted a female, and is usually directly preceded by an angel flight and bow (Fig. 1h). Frenzied flutters are also seen in the Blue-crowned Manakin (Lepidothrix coronata), the Red-headed Manakin, the Band-tailed Manakin (flutters), the Crimson-hooded Manakin, the Round-tailed Manakin, the Golden-headed Manakin, and the White-crowned Manakin (Robbins 1983; Tello 2001; Castro-Astor et al. 2004, 2007; Durães 2009; Prum 2010). This display is generally performed when a male is performing a solo display in the absence of a female, or shortly after a female leaves the display area without mating (Tello 2001; Castro-Astor et al. 2004; Durães 2009), and may be reminiscent of displacement behaviour common to other species after being thwarted during courtship (Tinbergen 1952; Moynihan 1955).

Dual back-and-forth In the absence of females, males occasionally face each other on parallel branches and perform back-and-forth as a dual-male display (McDonald, personal communication). They then take turns performing angel flights and bows towards each other, as if alternately imitating females.

Sequence and stereotypy of courtship display

We examined first order transitions between each display element to determine whether certain elements of the display were highly associated with other elements (i.e. whether they had high probabilities of preceding or following other elements). We found that some elements had high probabilities (>70 %) of repeating themselves, and some elements had high probabilities of directly transitioning to other specific elements (Fig. 2). For example, leapfrogs, back-and-forths, and tucked wing flicks all had high probabilities of repeating themselves, whereas lightning bolts and stationary displays had high probabilities of transitioning into upright postures and hopping displays, respectively. All display elements but one (frenzied flutter) had a reasonably high probability of directly preceding at least one other element (>10 % of the time); however, some elements had only very low probabilities of directly following other elements (<10 % of the time; see Fig. 2). Therefore, given that an individual element was performed, there was a reasonably high probability that at least one particular element was likely to follow it (e.g. an upright posture followed by a butterfly flight). However, the occurrence of some elements could not easily be predicted by the performance of any other elements directly preceding them (e.g. no display elements are highly likely to precede lightning bolts). Butterfly flights had high probabilities of both preceding and following the most display elements, with eight elements (including other butterfly flights) frequently preceding butterfly flights, and two frequently following them.

Fig. 2
figure2

Schematic of individual display elements of Long-tailed Manakin courtship display during all dances for females. Shaded boxes represent elements found within the hopping portion of the display; white boxes represent elements found within the butterfly portion of the display. Arrow thickness shows the probability that one display element follows another, based on the transitional probability matrix produced from 43 courtship displays for females, at 22 display areas. Note that some elements do not have high probabilities of following other elements, as they occur more rarely during displays (e.g. lightning bolts, back-and-forths, angel flights etc.). Therefore, a direct sequence may not be drawn from the beginning of the display through to the end (copulation) using only probabilities above 10 %. However, when considering transition probabilities of less than 10 %, paths exist between rarer elements, including butterfly flights and back-and-forths, and between back-and-forths and angel flights, which allows for a complete path through the courtship display

We observed a number of differences between matrices produced from all displays and matrices produced from only displays that contained copulations. When examining transitional probability matrices produced from all displays, some display elements were not highly associated with following any particular elements (e.g. darts only had high probabilities of following other darts, and angel flights and lightning bolts did not have high probabilities of following any other display elements). All copulations were directly preceded by bows; however, given that a bow was performed, there was only a 30 % probability that copulation would follow. When only considering transitions with higher than 10 % probability, we could not define a clear path from the beginning of the display to the end; however, including transitions lower than 10 % allowed for a complete path to exist. Although we could not detect a complete pathway through the display, we did find a moderate amount of structure at the first order level between individual display elements.

When examining transitional probability matrices produced only from successful courtship displays leading to copulation (Fig. 3), there were still several elements that were not highly associated with any other elements [e.g., darts had only low probabilities (<10 %) of following other elements, and lightning bolts had only low probabilities of following butterfly flights]. However, several other elements were more highly associated when including only displays with copulations. For example, back-and-forths had moderately high probabilities of preceding angel flights, though a complete path from the beginning of the display to the end was still not apparent when including only transitions with probabilities higher than 10 %. The probability that copulations would follow bows increased from 30 % when including all displays, to 83 % when including only successful displays; therefore, although bows were present before all copulations, multiple bows may occur within a successful display before females choose to copulate.

Fig. 3
figure3

Schematic of individual display elements of Long-tailed Manakin courtship display during successful dances for females. Shaded boxes represent elements found within the hopping portion of the display; white boxes represent elements found within the butterfly portion of the display. Arrow thickness shows the probability that one display element follows another, based on the transitional probability matrix produced from 18 courtship displays ending in copulations, at 7 display areas. Note that some elements are still not preceded by other elements with high probabilities, as they occur more rarely during displays (e.g. lightning bolts, back-and-forths, etc.). Therefore, a direct sequence may not be drawn from the beginning of the display through to the end (copulation) using only probabilities above 10 %. However, when considering transition probabilities of less than 10 %, paths exist between rarer elements, including butterfly flights and back-and-forths, allowing for a complete path through the courtship display

Long-tailed Manakin courtship displays for females also demonstrated a moderate level of structure at the second order, whereby certain display elements were highly likely to occur given that two specific elements directly preceded them. For example, given that a male performed a lightning bolt followed by an upright posture, there was a 95 % probability that a butterfly flight would follow (Table 1). Given the performance of an angel flight-bow combination, there was an 82 % probability that copulation would follow, though all copulations were preceded by an angel flight-bow combination. These results suggest that displays exhibit some structure at higher orders, though this pattern was not as pronounced as first-order transitions.

Table 1 Common second order transitions between elements of the Long-tailed Manakin Chiroxiphia linearis courtship displays performed for females, showing the probability a third element occurs given that two prior elements have been performed (all transitions with 0.70 probability or higher)

Variation in display and copulation success

Although parts of the courtship displays were highly stereotypical and structured, the fact that several elements were not highly associated with other elements suggests that there was still considerable variation in the structure of displays; that is, some elements of the display could follow or be followed by a variety of other display elements, allowing for considerable variation in structure within and among displays. Another source of variation that is not accounted for in the sequence analyses relates to the duration or rate of performance of display elements independent of order. Indeed, we found that the performance of Long-tailed Manakin display behaviours was highly variable among individual displays (Table 2). We were interested in investigating whether variation in specific display elements could predict copulation success during individual courtship displays (Table 2). We found that upright postures, bounces, angel flights, and bows all predicted successful courtship displays. Butterfly flights also approached significance in predicting copulations. Interestingly, butterfly flights were among the least variable display elements, while bounces, angel flights, and bows were among the most variable, though all display elements can be considered highly variable (Table 2). Given the stereotypy of the displays described above, it is important to note that many elements of the display were highly correlated (Table 3).

Table 2 Elements that predict mating success during 98 courtship displays of Long-tailed Manakins, as performed by definitive males for females, at 21 display areas
Table 3 Pairwise Spearman’s rank correlations of 14 elements of Long-tailed Manakin courtship display

Discussion

Our study provides the first detailed description of all visual elements comprising the complex, coordinated courtship display of Long-tailed Manakins. Our research also reveals that some elements of the display follow a highly stereotypical sequence, whereas other elements of the display appear to be more flexible in nature, resulting in considerable variation in structure within and among displays. In addition to varying the order of display elements, displaying males exhibit considerable variation in the duration or frequency of performance of individual elements, and for some particular elements this variation can predict copulation success.

Long-tailed Manakins exhibited a number of visual display elements that were similar to those of other manakins species. Several elements performed by Long-tailed Manakins were common to the genus Chiroxiphia, including variants of hopping, leapfrogs, butterfly displays, and buzz-weents (Gilliard 1959; Snow 1971; Foster 1981; DuVal 2007; Prum 2010). Furthermore, variants of the bow display occur in both Lance-tailed and Blue-backed Manakins, both of which also function as pre-copulatory displays (Snow 1963a; DuVal 2007). A number of display elements performed by Long-tailed Manakins were also similar to those performed in other manakin genera, including stationary displays, darts, upright postures, about faces, back-and-forths, and frenzied flutters (Snow 1963b; Robbins 1983; Théry 1990; Tello 2001; Rosselli et al. 2002; Castro-Astor et al. 2004, 2007; Durães 2009; Prum 2010). Recent phylogenetic analyses divided Piprinae manakins into two main tribes, and placed the genus Chiroxiphia within one monophyletic group (Ilicurini) alongside Antilophia, Illicura, Masius, and Corapipo (McKay et al. 2010; Ohlson et al. 2013). Darts and about faces were similar to displays exhibited by members of Corapipo, though no elements were shared exclusively by this genus (Théry 1990; Rosselli et al. 2002). Many display elements, including several of those shared by members of Chiroxiphia, had similarities with displays exhibited by members of Pipra, a genus included in the other tribe of manakins (Piprini), which also includes Xenopipo, Chloropipo, Lepidothrix, Heterocercus, Manacus, Machaeopterus, and Dixiphia (McKay et al. 2010; Ohlson et al. 2013). These observations suggest that some of these subcomponents may be basal elements of display among manakins, or that variants of these displays have evolved multiple times throughout the family (Prum 1997). Several other characteristics in this group are known to have evolved multiple times, including cooperative display, plumage patterns, and lek-breeding (Hellmayr 1910; Prum 1994, 1997, 2010; McKay et al. 2010). We also provide the first detailed description of angel flight displays, which were first mentioned by McDonald (2010); a similar behaviour is apparently exhibited by the closely related Lance-tailed Manakin (DuVal, personal communication). Although we have found no other records of similar displays in other manakins, full descriptions of courtship displays are not yet available for all species of manakin. Moreover, some display behaviours, such as angel flight displays, are so rapid and or subtle that they are difficult to detect in person; video recordings of manakin displays may reveal other undescribed displays in these species. For example, high speed video recordings of Golden-collared Manakins revealed display elements that were too difficult to detect at standard speed (Fusani et al. 2007). In addition, many descriptive accounts of manakin displays are brief and do not include detailed illustrations; therefore, it is difficult to determine whether certain elements of display differ significantly between species. Finally, it is unclear whether bill wiping is an actual element of the courtship display, a maintenance behaviour, a scent marking behaviour, or some other type of ritualized displacement behaviour (Tinbergen 1952; Scholes 2008).

We were interested in whether Long-tailed Manakin displays followed a stereotypical sequence. We found evidence that certain transitions between display elements were highly probable in both first and second order transitional probability matrices, suggesting that at least some components of Long-tailed Manakin displays are structured and stereotypical. Transitions between some elements were particularly stereotypical (e.g., angel flights to bows), suggesting that females may prefer certain combinations of elements more than the individual elements alone. Stereotypy is a common phenomenon in courtship (Tinbergen 1952); however, studies that quantify the level of stereotypy in displays are relatively rare. Previous research on the sequence of courtship display of the closely related Lance-tailed Manakin has revealed a highly structured display (DuVal 2007). For elements shared between Lance-tailed and Long-tailed Manakins, many of the same highly stereotypical transitions were observed, including the progression from hopping display to a buzz-weent homologue to butterfly display, as well as the transition from bow displays to copulations (DuVal 2007). A study on Zebra Finches (Taeniopygia guttata) demonstrated that dance displays tended to be stereotypical at the level of individuals and closely related family members, but not across all males (Williams 2001). A number of other avian studies report detailed accounts of stereotypical courtship displays, including Barbary Doves (Streptopelia risoria; Fusani et al. 1997), and Anna’s Hummingbirds (Calypte anna; Clark 2009). Like manakins, birds of paradise are known for their diverse and spectacular courtship displays (Scholes 2006). Detailed investigations of the behavioural patterns of birds of paradise have revealed high levels of structure and organization in the courtship displays of several Parotia species (Scholes 2006, 2007, 2008).

We found high levels of stereotypy within the Long-tailed Manakin courtship display; however, we could not demonstrate a direct sequence from start to finish (i.e. copulation) with high levels of probability (>10 %). A possible explanation is that copulations are a relatively rare occurrence among displays. Angel flights and bows always preceded copulations, but variation seems to exist between displays in how males manage to get to this point in the display. A recent study on Long-tailed Manakins demonstrated that aspects of female behaviour during courtship displays are correlated to copulation success (Ward 2012), suggesting that males may require feedback from females throughout the display before they attempt copulations. Previous research on Satin Bowerbirds (Ptilonorhynchus violaceus) demonstrated that males modulated the intensity level of their courtship displays based on behavioural cues from females (Uy et al. 2001; Patricelli et al. 2002, 2003, 2004, 2006). It is therefore possible that, in Long-tailed Manakins, an exact display sequence from start to finish cannot be defined, and that males may continue performing a particular set of display elements until proper cues are received from the female.

Studies that focus on overall ethological structure, rather than individual display elements may reveal important behavioural patterns that females use to choose mates. One study modified the display areas of Golden-collared Manakins (Manacus vitellinus) in such a way that the final pre-copulatory display element could not be performed properly (Coccon et al. 2012). Therefore, males were no longer able to perform successful courtship displays because the stereotypical sequence of courtship display was interrupted, which probably reduced the attractiveness of the display to females (Coccon et al. 2012). This type of study demonstrates the importance of understanding the structure of the courtship display as a whole; however, it is also important to understand how variation among displays can drastically affect the quality and outcome of these displays. Although we found stereotypy and structure in the courtship displays of Long-tailed Manakins, there was substantial variation in the performance of display elements among courtship displays, and this variation may influence copulation success.

We were interested in investigating the variation in performance of display elements between successful and unsuccessful courtship displays to determine whether specific display elements could predict copulation success. We examined courtship displays for females and found that upright postures, bounces, angel flights, and bows all predicted copulation success, and that butterfly flights approached significance in predicting copulations. This implies that upright postures, bounces, and butterfly flights may be particularly important in the display, whereas other elements (e.g. bill wipes, back-and-forths) may not be necessary to elicit copulations. Previous research conducted on the correlates of mating success in Long-tailed Manakins found length of butterfly and total length of display to predict copulation (McDonald 1989b; Ward 2012). Although we did not find length of display to directly predict copulation, upright postures, bounces, angel flights, bows, and butterfly flights were highly correlated with both the length of butterfly displays and the total length of displays (Table 3). In addition, butterfly flights were the most ubiquitous display element performed, followed by upright postures, and therefore they probably both contribute largely to the overall length of the display. Angel flights and bows are display elements that directly precede copulation, so it is not surprising that these elements predict copulation success, and bounces are highly correlated with angel flights, bows, and butterfly flights. However, if cues from females signalling willingness to mate are responsible for the onset of pre-copulatory display elements such as the angel flight and bow, it is possible that females are already prepared to mate, and may not necessarily be assessing these particular elements.

We found that the performance of all display elements was highly variable, which might be expected for behavioural displays in comparison to morphological traits, for example, but certain elements were more variable than others (Table 2). Back-and-forths and lightning bolts had the highest coefficients of variation, which may explain why few or no other elements had high probabilities of preceding them. Similarly, other rare display elements such as darts, angel flights, and bows, had high coefficients of variation. Butterfly flights had the lowest variation, possibly because they were performed so frequently and consistently throughout butterfly displays.

It is important to note that there were high correlations between many of the display elements occurring in the same display, and therefore it is difficult to determine which element, or combination of elements, may be responsible for influencing the mating success of courting males. For example, bounces, angel flights, and bows are highly correlated, as are upright postures and a number of flight elements including butterfly flights, darts, and lightning bolts. We demonstrated earlier that parts of the display are stereotypical in nature, and those elements of the display that are highly correlated are often elements that directly precede or follow one another. Perhaps females are not only cueing in on individual elements of the display but also how stereotypically the displays are performed by males. For example, females may be interested in upright postures, but perhaps they show stronger responses to upright postures directly preceded (or followed) by butterfly flights or darts. Certain combinations of display elements appear to be required, as all copulations were preceded by angel flight–bow combinations. Although there is variation between individual courtship displays, reinforcement from choosy females has likely shaped the evolution of stereotypical displays in this species.

High levels of individual variation between displaying males, and thus high variance in copulation success is common among lekking species (Bradbury 1981; Bradbury and Gibson 1983; Höglund and Alatalo 1995). Although courtship display may be highly ritualized, females can detect minute differences in attractive components of displays (Bradbury and Gibson 1983). Therefore, understanding variation at the level of individual subcomponents, as well as the display as a whole, has important implications for understanding mate choice. In lekking species, all parental care is provided by females; therefore, females likely choose males based on the potential of gaining indirect fitness benefits for their offspring (Bradbury and Gibson 1983; Kodric-Brown and Brown 1984; Kirkpatrick and Ryan 1991). In Golden-collared Manakins, females prefer males that perform certain courtship elements at higher speeds, which likely reflect agility and stamina (Barske et al. 2011). In Long-tailed Manakins, the performance of display elements such as upright postures, bounces, angel flights, and bows may indicate superior genetic quality to females, which could be based on rate of display, stereotypy, energetic requirements, or coordination with other males. Further research on how females assess these particular display elements will contribute to our understanding of the underlying mechanisms of mate choice in this species.

Our research provides the first detailed characterization of courtship display in Long-tailed Manakins, and also demonstrates that some elements of the courtship display are highly stereotyped in this species. Nevertheless, displaying males exhibited high levels of variation in the performance of display elements among courtship displays for females, and we demonstrate that the performance of several display elements predicts mating success. This research may enhance our understanding of how mate choice influences the evolution of a highly complex and stereotyped courtship display.

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Acknowledgments

This project was funded by a Student Research Award from the Animal Behavior Society (to K.C.L.), a Natural Sciences and Engineering Research Council (NSERC) of Canada Discovery Grant (to S.M.D.), and the University of Windsor. We would like to thank the park staff of the Área de Conservación Guanacaste (ACG) for logistical support, with special thanks to Roger Blanco. We are grateful to K.-A. Ward for assistance in the field, R. Verraich and S. Burton for assistance with video analyses, and P.-P. Bitton, K. Gammie, D. Mennill, Associate Editor L. Fusani, E. DuVal, and one anonymous reviewer for comments on the manuscript. The methods of data collection used in this study comply with the current laws of Costa Rica and Canada.

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Correspondence to K. C. Lukianchuk.

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Online Resource 1 Video of Long-tailed Manakin (Chiroxiphia linearis) courtship display, performed by two definitive males for a female. The video begins with dual hopping display, followed by dual and solo butterfly display performances, ending in copulation. The video comprises a single successful courtship display but the displaying males do not exhibit all 16 elements of the courtship. The video has been edited to remove long segments of repetitive display elements and therefore does not reflect the actual length of the display.

Supplementary material 1 (MPG 82512 kb)

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Lukianchuk, K.C., Doucet, S.M. Cooperative courtship display in Long-tailed Manakins Chiroxiphia linearis: predictors of courtship success revealed through full characterization of display. J Ornithol 155, 729–743 (2014). https://doi.org/10.1007/s10336-014-1059-3

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Keywords

  • Courtship display
  • Courtship success
  • Chiroxiphia
  • Sequence
  • Stereotypy
  • Manakin