Individual and temporal variation in cloacal protuberance size of male Bearded Tits (Panurus biarmicus)

ANDREAS SAX 1 AND HERBERT HOI

ABSTRACT.-The intensity of sperm competition is one of the factors known to determine interspecific variation in the size of male reproductive organs. However, individual variation in the size of reproductive organs and its relation to male quality have not been considered appropriately. We investigated the annual pattern of variation in the size of the cloacal protuberance (CP) in male Bearded Tits (Panurus biarmicus) and correlated CP volume during the fertile period of females with reproductive and morphological features of males. Contrary to other passerines, the cloacal protuberance does not constitute a sperm reservoir but functions as a copulatory organ in Bearded Tits. CP volume differed significantly between unmated and mated males and provided a good indicator of their reproductive status. Within individual mated Bearded Tits, CP size changed in conjunction with their mate's fertile cycle, peaking around the day of clutch initiation. During the fertile period, mated Bearded Tits possess the largest CP (relative to body size) known for a passerine (average volume index = 59.14 mm3 per g; n = 16). The adaptive value of this feature could be that it improves ejaculate transfer owing to better and longer cloacal contact. Relative to unmated males, mated males have more total sperm stored in their seminal glomera and larger testes, suggesting the occurrence of large disadvantages for unmated males to gain reproductive success. An isolation experiment showed that female presence positively influences the development of CP size in virgin male Bearded Tits. Received 14 April 1997, accepted 12 March 1998.

SPERM COMPETITION is widespread among animals (Parker 1970, Birkhead and Moller 1992) and has a profound effect on the behavior and morphology of a variety of species (LeBoeuf 1974, Clutton-Brock et al. 1980, Birkhead et al. 1987, Davies 1992). Much of the variation in the size of traits related to reproduction can be accounted for by the intensity of sperm competition (McKinney et al. 1984; Cartar 1985; Moller 1988, 1991; Birkhead et al. 1991; Briskie 1993; Schulze-Hagen et al. 1995; Rising 1996). Contrary to many other vertebrates, most male birds (exceptions include ratites and waterfowl) do not possess an intromittent copulatory organ (Lake 1981). The external sexual organ is usually restricted to a swelling of the cloaca, the so-called cloacal protuberance (CP), which is caused by the growth of the seminal glomera (Salt 1954) that function as the site for the storage and maturation of sperm (Wolfson 1954, Lake 1981). Interspecific variation in relative CP size is best explained by the sperm-competition hypothesis, which predicts that when sperm competition is intense, a large protuberance is required for the maintenance of sufficient numbers of sperm (Birkhead et al. 1993). Wolfson (1954, 1960) also suggested that the CP could act as a phallus or at least facilitate copulation. The latter suggestion seems to be particularly relevant for the Bearded Tit (Panurus biarmicus), which is unique among passerines in that the CP does not represent the coiled seminal glomera, but consists of a muscular layer and terminates in a small papilla (Birkhead and Hoi 1994). Birkhead and Hoi (1994) thus concluded that in Bearded Tits, the CP forms a copulatory organ.

Because the development and maintenance of morphological features can be costly, the relative size of such characters may function as a cue to the respective male's quality (Sheldon 1994). Studies of morphological features associated with reproduction, such as antlers (Clutton-Brock 1980) and plumage (Petrie et al. 1991), have illustrated the significance of studies at the level of the individual. We examined the morphological and functional differences in the CP in a population of Bearded Tits. Specifically, we: (1) examined seasonal patterns of male CP development over the breeding period, at both the species and the individual level; (2) evaluated possible individual variation in CP size; and (3) related such variation to male reproductive parameters and to morphological features important in female choice.

The social system, sexual strategies, and reproductive parameters of Bearded Tits are known in some detail (Hoi 1989, Birkhead and Hoi 1994, Hoi and Hoi-Leitner 1997). Bearded Tits are socially monogamous, nonterritorial passerines of Eurasian "reed belts," where individuals form pair bonds while they are still juveniles (Koenig 1943). Males possess black feathers that form stripes under each eye, the so-called "beard." The beard, along with tail length in males, function as cues in mate choice by females (Hoi unpubl. data). Because the species shows a male-biased sex ratio of 2:1 throughout the breeding season, flocks of unmated males occur regularly (Hoi 1989). From mid-March until July, pairs produce up to four clutches (Bibby 1983). Copulation frequency is high, with up to 200 copulations per clutch (Hoi 1997). Many of the copulations are solicited by females that initiate "chase-flights" in which up to 13 males follow the soliciting female (Koenig 1943). As a consequence, extrapair copulations and extrapair paternity are rather high in Bearded Tits (Hoi 1997, Hoi and Hoi-Leitner 1997).