Distinctive courtship phenotype of the Vogelkop Superb Bird-of-Paradise Lophorina niedda Mayr, 1930 confirms new species status

Advertisement display

The central features of this display involve the male excitedly looking up and around from side to side (presumably for a potential mate) while repeatedly flicking his cape forward in front of his head and calling (video vouchers: superba ML458000 from 0:44 to end; niedda ML487533). Upon arrival to the fallen log used for display, the male stands in an alert upright posture with head up, bill forward and tail down (Figs. 1A & 1B and S1A). The iridescent crown feathers are pushed (anteriorly) toward the bill so that they do not visibly reflect any blue and the entire head appears black from all directions. In this configuration, the ornamental eye-spots are not visible (Figs. 1A & 1B and S1A & S1B). In niedda, the male typically arrives and departs from his display log by flying low through the forest understory rather than by dropping down from or flying up to the forest canopy immediately above. It is unclear if superba does the same with the available data.

In superba, the main posture of the advertisement display has the nape cape folded over the back and wings, without being spread, such that the terminal tips of the cape reach to, or extend beyond, the base of the tail completely covering the wings (Fig. 1A). In neidda, the configuration differs in that the cape sits spread over the upper back such that the terminal tips extend conspicuously to the sides leaving the wing tips and base of the tail uncovered (Fig. 1B).

In superba, the feathers of the breast shield are held close to the breast and upper body so that, for the most part, the color of the ornament is not visible, especially as viewed from above (Figs. 1A and S1A). One exception is during high-intensity calling in which case the breast is thrust forward causing the breast shield to be pushed outward and made visible (Fig. S1B). In contrast, the breast shield of neidda is not held as tightly against the breast and its shorter and narrower lateral tips do not fold back toward the torso as in superba (Fig. 1B). The terminal tips of the neidda breast shield curve gently outward, which makes the surface of the breast shield slightly concave (Fig. 1B). In both superba and niedda, the bright yellow color of the gape becomes visible while calling (Figs. 1A & 1B and S1B).

Beyond repeated side to side head turning, the primary movements of the display are a frequent forward “flicking” of the cape, which results from turning the head down and to the side and into a partially open wing in order to perform a rapid false wing preen motion (Figs. 1C and 1D). The extremely fast movement of the false-preen causes the cape to be quickly flicked forward over the downward turned head in a highly exaggerated and ritualized fashion. In superba, the cape largely retains its compact form when flicked forward whereas in niedda, the flicked cape is fanned out over the head (Figs. 1C and 1D).

Horizontal display

This display is frequently interspersed throughout bouts of the advertisement display and involves the diagnostic adoption of a rigid horizontal posture with the neck outstretched, head lowered, and bill pointing forward to be in line with the body axis (video vouchers: superba ML458000 (from 0:33–0:44) and ML458001 (from 0:27–0:34); niedda ML487558 from 0:00–0:30). The tail is also lifted so that the whole body forms a horizontal line from tip of the bill to tip of the tail (Figs. 2 and S1C).

In most instances, the crown feathers are pushed forward so that the head remains all black in appearance and the ornamental eye-spots are not visible (Fig. 2). However, the eye-spots are occasionally revealed during practice displays or if the bird is about to transition into the pointing display (see below), but then concealed again as the horizontal display continues or the bird ruffles its plumage and returns to a bout of advertisement display.

In superba, the cape is folded over the back to the base of the tail and is not spread (Figs. 2A and S1C). In a position that creates a very different appearance, the cape of niedda is held over the back, but spread so that it forms two decurved “wings” that emanate from each side and with tips that droop to the log (Fig. 2B). At times, the cape is partially lifted over the back so that it forms a slight arch behind the head.

In superba, the longest (lateral) feathers of the breast shield stick out conspicuously to the sides and the central most breast feathers are sleeked against the body so that no color is visible, especially when viewed from above (Fig. 2). Because the body is in elongated horizontal posture, only the blackish underside (ventral side) of the breast feathers project outward. The dark outwardly pointed tips give the appearance of being small pointy “wings” sticking out from the sides of the breast. In niedda, the breast shield is also sleeked against the body with no color visible (Fig. 2B), however unlike the arrangement in superba, the longest breast shield feathers do not look like “wings” because the wing-like position of the cape obscures them (Fig. 2B).

The main movement of the horizontal display is ritualized hopping “run” along the log to change position and orientation (e.g., see ML487557 from 1:16 to end and ML487563 from 0:00–0:25). The hops use both feet at the same time and are typically initiated with a quick wing-flick just prior to the first hop. Although less frequent than in advertisement display, the false wing-preens that cause frontal cape flicking are also given.

Pointing display

The final display in the initial display activity sequence begins from the posture of the horizontal display, which is the most common, or following an advertisement display vocalization. As the name suggests, the primary feature of this display involves the adoption of a ritualized pointing posture where the bill points skyward as the male’s attention is oriented toward a potential, or actual, female (video vouchers: superba ML458002 from 0:22–0:53 and ML458003 from 0:50–0:56; niedda ML487538 from 0:00–0:03 and ML487540 from 2:10–2:23). In superba, the body is held in an upright posture, with the upper body lifted from the horizontal to be erect as if the bird is “standing at attention” (Fig. 3A). In niedda, body posture is more horizontal with the upper body closer to the log and the head tilted back so that the bill points upward (Figs. 3B and 4).

A key feature of this display is how the feathers of the fore crown are pushed back (posteriorly) to be flattened against forehead the while the hind crown feathers remain pushed forward (anteriorly). This result of this repositioning is that the highly reflective fore crown feathers become visible, changing the appearance from all-black to an iridescent electric blue (Figs. 3 and 4). At the same time, the feathers of the narial tufts are also pushed outward from both sides of the bill, which when aligned with the blue fore crown feathers, and viewed head-on, create the highly distinctive eye-spot ornament. When visible, the eye-spots reflect so brightly relative to the super-black plumage surrounding them that they look somewhat like a pair of headlights (Figs. 3 and 4). It should also be noted that the shape of the erected narial tufts differs between niedda and superba. In superba, the tufts are shorter and thicker, almost wedge-shaped, and do not extend beyond the width of the head (Fig. 3A). In niedda, the tufts are narrow and elongate with tips that extend out beyond the width of the head (Fig. 3B).

As with the previous behaviors, the arrangement of the cape differs substantially between superba and niedda. In superba, the cape remains tightly folded over the back and is not noticeably spread (Fig. 3A). In niedda, the cape is always prominently spread broadly over the back to form the conspicuous decurved wing-like lateral protrusions that are a hallmark of the niedda courtship phenotype (Fig. 3B).

During the pointing display, the breast shield of superba, though not as outstretched as in the cape presentation display (see below), is nevertheless quite prominent with its reflective blue color visible (Figs. 3A and S1D). In niedda, the breast shield remains sleeked against the breast and largely invisible—its lateral tips concealed (shadowed) by the protruding “wings” of the cape—when viewed from the vantage point of an approaching female (Fig. 4).

The main movements during the pointing display involve a ritualized flapping of the cape up-and-down over the back and occasional reorientation along the log to “track” the position of a female as she moves around nearby or approaches. The details of the cape-flap differ between superba and niedda. In superba the cape-flap occurs when the wings are partially lifted and flicked open over the back in coordination with a quick pronounced foot stomp, which causes the cape to flap up-and-down over the back in an exaggerated way such that the terminal tips of the cape feathers rise above the height the of the head (Fig. 3C). In niedda, there is a foot stomp, but wings are not flicked open, and are only just raised slightly up-and-down over the back, which results in the cape flapping up, but not as high, and such that the terminal tips of the cape feathers stay at or below the level of the head (Fig. 4D).

If the pointing display does not transition into a bout of high intensity display (see below), the fore crown feathers may be pushed forward and back, which causes the eye-spots to disappear and reappear or to “flash” on and off. In that scenario, the breast shield of superba is sometimes sleeked against the body again, which cause the reflective blue color to visually “blink off” as well. The cape-flapping may also revert into the pseudo wing-preen cape flicks that are a common feature of the advertisement display.

A noteworthy behavior associated with the initial display activity of niedda is a leaf tossing behavior (e.g., ML487565 from 1:24–1:35). For this behavior, the male picks up a leaf from the surface of the display log and tosses it into the air in such a way that it often lands on the log nearby. It is unclear if this behavior is a rudimentary form of court clearing behavior similar to that known from Parotia species or if it is some form of ritualized visual display like those of Parotia carolae, which uses leaves as props during certain displays (Scholes, 2006).

Cape presentation display

The visual form and movements of this display comprise the quintessential features of courtship in the genus Lophorina (video vouchers: superba ML458003; niedda ML487557 and ML487562). When performed to a female, the cape presentation display is typically initiated from the posture of the pointing display—i.e., Fig. 3A superba and Figs. 3B and 4 niedda). However, if a female appears suddenly without stopping on a nearby perch on her approach, and during practice displays (no female present), the male will often transition directly into the cape presentation from any of initial display activities (e.g., in ML487557 the pointing display is omitted and the male appears to be caught off guard by the sudden arrival of the female).

The cape presentation display begins when the male perceives a female making her approach toward the log. In both superba and niedda, the cape-flapping of the pointing display (see above) increases in intensity. In niedda, the increase is greater as wings are lifted higher over the back and then quickly flicked open and shut in the exaggerated manner of superba during pointing (Figs. 5A and 5B). As in the pointing of superba, the cape feathers of niedda also flap higher such that the tips exceed the height the of the upward pointing bill (Fig. 5B). In conjunction with the exaggerated wing-flick/cape-flaps, the head is tilted back more sharply, the bill is also opened widely to reveal the bright yellow gape and the breast is thrust forward so that the feathers of breast shield ornament become fully expanded and conspicuous—its reflective surface angled upward toward the approaching female (Figs. 5A and 5B). The point at which the male presents his bright yellow gape is the best landmark for identifying of the start of the cape presentation display even though there is often a bout of the exaggerated wing-flick/cape-flaps preceding it.

The visual effect of the exaggerated wing-flick/cape-flaps with the breast shield fully revealed is more pronounced in niedda than superba because of the stark difference in the appearance of the breast shield during the pointing display (e.g., compare breast shield positions in Figs. 3A and 3B to those in Figs. 5A and 5B). In both species, the male will reorient himself as needed to track the position of the approaching female and keep his eye-spots and breast shield directed toward the female (e.g., video ML487530).

In niedda, bouts of wing-flick/cape-flapping coincide with a distinctive very rapid side-to-side wobbling of the head. As viewed from the front (i.e., the POV of the approaching female) the head wobbling has the effect of making the eye-spots flicker or shimmer. It is possible that the wobbling head movement may also be present in superba, but is not discernible from the available data.

Next comes the transition into the main part of cape presentation display—i.e., the presentation of the fully opened cape itself. In superba, the cape is lifted into its presentation position well before to female arrives on the log (Fig. 5C). In L. niedda, the wing-flick/cape-flaps with head wobbles continue for several more bouts after the female has arrived on the log and approaches the male become face-to-face with him (Fig. 5D). As the neidda female moves closer, the male will back up slightly and crouch lower before deploying his cape for full presentation (e.g., videos ML487530, ML487538, and ML487562).

Although the timing of cape deployment differs between superba and niedda, the cape of both is lifted into the full display position in largely the same way. First, it is spread wide, fan-like, over the back and then it is raised (anteriorly) and pushed over the head until it creates the super-black (McCoy et al., 2018), slightly concave, cape presentation display form that surrounds the entire head and upper body (Figs. 5E & 5F and S1E).

Once in position however, the form and appearance of the cape presentation phenotype differs dramatically between superba and niedda. In superba, the shape of the cape presentation form is oval—i.e., wider than it is high (Figs. 6A & S1F). In comparison, the shape of the cape presentation form of niedda is distinctly crescent shaped—i.e., it has a curved sickle shape that is broad in the center and tapers to a point at each end (Fig. 6B). In superba, the border edge of the fully opened cape has a smooth fuzzy appearance (Fig. 6A), which is created by the distinct hair-like fringing along the terminal tips of the individual feathers that comprise the cape. The border edge of the crescent in niedda is slightly ribbed and lacks the fuzzy appearance of superba (Fig. 6B). Correspondingly, the terminal tips of the niedda cape feathers have very minor hair-like fringing. The iconic oval shape of superba exhibits very little variation within the superba complex (e.g., Fig. 6A and Fig. S1F for a comparison of L. s. latipennis and L. s. superba and refer to the documentary films described in the Methods for comparative imagery of L. s. addenda).

The shape and appearance of the breast shield also differs between the cape presentation phenotype of superba and neidda. In superba, the breast shield is wider with thicker terminal ends that make a relatively flat surface with a fairly straight edge along the top of the ornament (Fig. 6A). In neidda, the shorter and narrower terminal tips of the breast shield curve outward so that the surface of the ornament is slightly concave and the top edge is angled downward at the sides (Fig. 6B). This difference results in niedda looking like somewhat like “frowning face” whereas superba has a “smiling face” look. The “smiling” vs “frowning” face appearance is further enhanced by the difference in how the eye-spot ornaments are created. In superba, the the narial tufts are thick and relatively short whereas in niedda they are narrow and longer (i.e., extend beyond the width of the head). This difference has the effect of making the eye-spots of niedda appear smaller with a straighter line along the top edge, which gives the “eyes” the appearance of having slightly droopy “eyelids” compared with the always larger and circular appearance of the “eyes” in superba (Figs. 6A and 6B). In addition, when alignment of the feathers is not perfect relative to the viewer, the thinner profile of the narial tufts often makes the eye-spots of niedda look like they have a thin blue “eyebrow” just above each eye-spots (Fig. partially visible in Fig. 5F). Because the narial tufts fo superba are shorter and do not extend over the top margin of the eye-spot, “eyebrows” are never visible nor even possible.

Throughout the cape presentation display, the transformed oval-shaped cape presentation form of superba is repeatedly lifted up and down, or bounced, with outstretched and bent legs (e.g., ML458003). The repeated up and down movements coincide with a series of alternating shuffle–hop steps to the side, which create the distinct bouncing cadence: up–down shuffle–hop, first to one side and then the other. When a female is present, the male’s bouncing shuffle–hop movements revolve around the female in either a semi-circular or full circle path.

In niedda, the overall appearance of the rotational movement during the cape presentation display is very different from that of superba. Instead of the characteristic bouncing of superba, the feet of niedda move in a faster, more pronounced, side-step motion without bouncing and with no visible up and down movement of the body. This creates the effect of niedda appearing to move in a quick but steady glide, rather than bounce, around the female in semi- or full circle (e.g., ML487557 and ML487562).

Along with the bouncing (superba) or smooth quick (niedda) rotational movement of the cape presentation form along the display log, the tail of both species is lifted to about 45 degrees above the plane of the back and rectrices are fanned. The secondary feathers of the wings are spread such that they become partially intertwined with the rectrices (see Fig. S1E). In one explosive motion, the wings are flicked open and shut to the sides, which causes a violent interaction among the secondaries and rectrices. In superba, the explosive wing-flicks occur rhythmically with the up–down bouncing movement and coincides with the distinct snapping sounds that are a characteristic acoustic component of the display. In superba, the wing-flicks happen on the “down beat” of the bounces, but not on every bounce. In s. latipennis, the cadence of snaps and bouncing is down-snap-up, down-snap-up, down-up such that snaps occur in doublets with a distinct pause in between, which sounds like “snap-snap (pause) snap-snap” (Fig. 7A). In niedda, where the rotational movement lacks the bouncing of superba, the overall pattern and effect of the wing/tail flicks and snaps is very different because they occur at a regular interval that is not timed with any particular aspect of the rotational movement. The snaps of niedda are given at uniform beat of approximately one snap per second for a steady “snap-snap-snap” sound (Fig. 8B).

In s. superba, the cadence of the snapping is more frequent with less obvious choreography among the snaps and bouncing movements. In s. addenda, to the extent discernible from the documentary video sources, both the cadence of the bouncing and snapping seems to be more frequent with wing-flicks (and presumably the snaps) occurring with each downward bouncing stroke, “down-snap-up, down-snap-up, down-snap-up”. In both niedda and superba, the exact relationship between the wing movement and snapping sound production is unclear and warrants further investigation using high-speed videography.

In both superba and niedda, the cape presentation display ends when the female moves quickly away from the male such that he is unable to continue rotating around her, or when the female solicits copulation. At times the female moves along the log ahead of the male and at other times she will fly away from the log entirely. When females depart, males of both superba and niedda maintain the full cape presentation posture directed toward her and slowly lower it down over the back to readopt the pointing posture. In niedda, as the female departs, the male opens his bill to reveal the bright yellow gape once again. This end of display reveal of the gape was not observed in superba.

If a female solicits copulation (e.g., ML487568 from 0:07–0:17), she beings fluttering her wings as the male rotates around her and then will tip forward with breast low and tail high. At this point, the male circles closely and mounts the female while maintaining the fully open cape posture. The cape is held in the open position during copulation and wing-snaps are given as part of, or just after, the wing flapping that occurs with copulation. After copulation, the male dismounts from the back of the female and resumes the cape presentation display directed at the female (e.g., ML487562). If she departs the log, the male holds the opened cape posture for a few seconds and the slowly lowers it and often returns to the pointing display and sometimes even reverts backwards through the entire sequence from pointing, to horizontal to advertisement displays.