The males of very few bird species possess a penis1. Buffalo weavers, Bubalornis spp., are unique in possessing a false penis, or phalloid organ2,3. We find that, after protracted copulation, the phalloid organ generates an orgasm-like state in males, a phenomenon not known in any other bird. The possession of a phalloid organ and orgasm may be associated with the buffalo weaver's unusual mating system in which there is intense sperm competition.
We studied individually colour-ringed red-billed buffalo weavers, B. niger (Fig. 1a), in Namibia. The phalloid organ is a stiff rod of connective tissue 15.7±0.29 (s.e.) mm long (n =109) that lies immediately anterior to the cloaca (Fig. 1b). It has no ducts2,3 and is not homologous to any penis found in any other bird species1. Females have a much smaller phalloid organ (6.1±0.19 mm long, n =68).
The buffalo weavers bred in colonies of 5.7±1.1 nests (n =24), with each nest containing 6.5±0.8 (n =16) chambers, of which 4.6±0.7 (n =13) were occupied by a single female. Of ten nests studied, two were defended by one male, and eight by two males who appeared to operate as a coalition: both males built the nest, defended it against other males, and fed the chicks in all nest chambers. The mating system was therefore either polygyny or, at two-male nests, cooperative polygynandry.
Multilocus DNA fingerprinting4 of ten male coalitions revealed that in only one instance were males probably first-order relatives (brothers, or father and son); in at least seven other cases, coalition males appeared to be completely unrelated. Sperm competition was intense. Multilocus DNA fingerprinting of 55 offspring from 25 broods indicated that, in 18 broods (72%), offspring either had more than one father or included offspring fathered by non-resident males.
Copulations were difficult to observe because they occurred between 75 and 500 metres from the nest in dense tree cover. Six complete sequences were protracted (mean 18.0 min, range 4-30 min) and comprised alternating sequences of ‘bouncing’ displays by both sexes and mounting. It was impossible to establish the position or role of the phalloid organ during copulation as it was obscured by feathers. We therefore caught (under licence) 13 males and 6 females, transported them to Germany and kept them in aviaries, where we observed 57 copulations between three males and five females. In captivity, males also copulated 34 times with a taxidermist's mounted female with an artificial cloaca5 (a ‘model female’), which we placed inside the aviary.
Mounting was similar to that in other birds, with the male on the female's back. But as copulation proceeded, the male usually adopted a reclining position, leaning backwards away from the female (Fig. 1c). Contrary to earlier speculation1,3, the phalloid organ was not intromittent, but instead appeared to be rubbed against the female's cloacal region. As in the wild, mounting bouts were prolonged (29.0±0.76 min, n =34). In the final stages of copulation, males appeared to experience an orgasm during which the male's wing beat slowed to a quiver and his entire body shook; with his leg muscles apparently in spasm, his feet clenched hold of the female and drew her towards him. The behaviour of males copulating with the model female was similar, and only in those instances when males experienced an orgasm (n =34) was semen found in the false cloaca, suggesting that orgasm is necessary for ejaculation.
To test the idea that protracted mounting and physical stimulation of the phalloid organ results in orgasm and ejaculation, we rubbed the phalloid organ of each of three males (on two separate occasions each) immediately after they had copulated with and inseminated a live female. All three ejaculated almost immediately each time; similar stimulation without mounting was ineffective.
Our results indicate that the phalloid organ is a stimulatory organ that may have evolved in response to the intense sperm competition mediated, in part, by a polygynandrous mating system. Unusual copulation behaviour occurs in other birds with intense sperm competition6,7. The way in which a stimulatory phalloid organ increases male reproductive success remains unclear, however. One possibility is that, as in some rodents8, repeated mounting and protracted physical stimulation of the male, and consequently the female, before ejaculation increases the likelihood that a female will retain and utilize his sperm.
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Winterbottom, M., Burke, T. & Birkhead, T. A stimulatory phalloid organ in a weaver bird. Nature 399, 28 (1999). https://doi.org/10.1038/19884
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