Song Learning in Brood-Parasitic Indigobirds Vidua Chalybeata: Song Mimicry of the Host Species
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Anim. Behav., 1998, 55, 1537–1553 Song learning in brood-parasitic indigobirds Vidua chalybeata: song mimicry of the host species ROBERT B. PAYNE, LAURA L. PAYNE & JEAN L. WOODS Museum of Zoology and Department of Biology, University of Michigan (Received 18 March 1997; initial acceptance 22 June 1997; final acceptance 5 September 1997; MS. number: 7694) Abstract. Brood-parasitic village indigobirds, Vidua chalybeata, were bred in captivity and foster-reared by their normal host, red-billed firefinch, Lagonosticta senegala, or by an experimental foster species, Bengalese finch, Lonchura striata. Male indigobirds reared by Bengalese finches developed the songs of Bengalese finches, and males reared by firefinches developed songs of firefinches. Males copied their foster father only when they had lived with him long after independence (45 days post-fledging), while males separated normally at independence (22–24 days post-fledging) copied songs of other individuals and not songs of their foster father. Males reared by Bengalese finches showed no preference to learn firefinch song over songs of the experimental foster species or other control finch species even when they had lived with firefinches as companions from the time of fledging to independence. Males copied several song themes, acquired the same number of mimicry songs, and acquired their songs at the same age, whether reared by Bengalese finches or by firefinches. When they lived with other indigobirds, the male indigobirds copied mimicry songs of male indigobirds that mimicked the same foster species. We predicted mimicry-song specificity and repertoire size in experimental indigobirds from a hypothesis of an early developmental period when young indigobirds focus their attention on their foster parents, and a later period when they direct their attention to other birds with similar songs. The predictions, based on field observations of wild birds, were that (1) males reared by a novel foster species other than the normal host would learn the song of that foster species, and (2) males that left their foster parents at the normal time of independence would copy the songs of other individuals, including other adult indigobirds that mimicked the same foster species. Begging calls of young indigobirds did not mimic the calls of young firefinches. Indigobirds reared alone, or with young of the normal host or of the experimental foster species, all developed begging calls in adult song that resembled their own begging as nestlings and fledglings, and only males that heard other adult indigobirds with firefinch-mimicry begging developed firefinch begging in their song. The incorporation of the innate begging calls as well as the learned begging calls into adult song, and the modification of the song themes of their individual song models, suggest that song development involves processes in addition to copying the songs of their own foster species and of older adult male indigobirds with songs like their own foster parents. 1998 The Association for the Study of Animal Behaviour The African village indigobird, Vidua chalybeata, in the songs they mimic. Each indigobird species is a brood-parasitic songbird. Adult male indigo- parasitizes a different host species, and each birds mimic the songs and begging calls of their male’s mimicry songs indicate his own species host species, the red-billed firefinch, Lagonosticta identity as well as his foster species (Payne 1973, senegala, and female indigobirds visit and mate 1983, 1996; Payne & Payne 1994, 1995). The with males that mimic the song of their host brood-parasitic nestlings also mimic the host nest- species (Payne 1973, 1990). Although the breeding lings in mouth pattern and colour (i.e. each brood plumage of male Vidua indigobirds differs only parasite–host species pair displays a different slightly in colour, the species differ conspicuously mouth pattern), which may allow the nestlings to Correspondence: R. B. Payne, Museum of Zoology, be accepted in the host brood and receive the care University of Michigan, Ann Arbor, MI 48109-1979, of a discriminating foster parent (Nicolai 1964; U.S.A. (email: [email protected]). Payne 1996). In contrast, while the ‘begging calls’ 0003–3472/98/061537+17 $25.00/0/ar970701 1998 The Association for the Study of Animal Behaviour 1537 1538 Animal Behaviour, 55, 6 of adult indigobirds appear to resemble those of 1996). Straw-tailed whydah, V. fischeri, another their host species (i.e. ‘begging calls’ in adult brood-parasitic finch that mimics the songs of mimicry song; Nicolai 1964; Payne 1973), the its host species in the field (purple grenadier, begging calls of dependent indigobirds recently Granatina ianthinogaster), copied the songs of recorded in the field differ from those of their host Bengalese finch, Lonchura striata, when reared by species (Payne 1996). Insofar as a male indigobird it in experimental conditions; whydahs copied mimics the species that reared him and this song both the foster father and other male Bengalese mimicry is learned, his songs inform the female finches (Nicolai 1973). about his own early experience and function as a Field observations suggest that male indigo- sexually selected signal to the female of the genetic birds learn their mimicry songs, but they do not quality of the male. If she mates with a male learn only from their foster parents. Each adult whose mimicry songs are like those of her own male indigobird has a repertoire of three or four foster parents, then the pair will produce offspring mimicry songs, rather than one or two as expected having a mouth pattern that matches their if he simply had the songs of his foster parents common host species. (a male firefinch usually has one song theme, a Learning the songs of the host species may also female has one song theme but a female rarely be important in colonization of a new host and in sings, Payne 1990). Neighbouring male indigo- speciation. If males learn the song of their own birds match the details of all three or four mimicry foster species, then song learning may be part of songs with each other. Because firefinches are the process through which indigobirds success- individualistic in song and the indigobirds are not fully colonize a new species of host, as follows. (Payne 1979, 1985, 1990), it is likely that male Colonization may begin when an errant female indigobirds copy their mimicry songs from lays in the nest of a novel foster species and her another male indigobird rather than from their young survive, the males reared by the new foster own firefinch foster parents. Their population copy the songs of the novel host, and females are ecology also makes it unlikely that all male indi- attracted to males with songs like their own gobirds in a neighbourhood would have the same foster parents and lay in the nests of their own foster parents: indigobirds parasitize about 30% foster species. The process of host switching and of the firefinch nests (Morel 1973; Payne 1977) mimicry of the new host’s songs may lead to and indigobirds that match each other’s mimicry indigobird speciation when genetic differences songs are only about 10% as numerous as fire- accumulate through selection between the finches within the same area (Payne & Payne descendants of parasites on old and new hosts 1977). In addition, a few male village indigobirds (Payne 1973; Payne & Payne 1994). Molecular (1%) do not mimic the songs of red-billed firefinch and morphological evidence suggest that indigo- but mimic the songs of another species of finch; birds colonized their host species well after the these may be males that were reared by the other host species had diverged, rather than having species (Payne 1973; Payne et al. 1992, 1993). co-speciated along with them (Payne et al. 1993; Also, juvenile indigobirds reared and captured in Klein & Payne 1998; Payne 1998). the field in Zambia and then kept with firefinches Although indigobirds may learn mimicry songs from another part of Africa copied the individu- and calls from their foster parents, the evidence is alistic songs of these novel firefinches. When the indirect, based on the widespread occurrence of indigobirds sang as adults, their novel mimicry song learning in songbirds (Kroodsma & Baylis songs were copied by other yearling indigobirds 1982) including the estrildid finches, the group to from Zambia (Payne 1985). which the Vidua finches are perhaps most closely A hypothesis to account for the learning of related (e.g. Goodwin 1960; Gu¨ttinger 1972, 1973; mimicry songs and the matching of mimicry songs Gu¨ttinger & Achermann 1972; Dietrich 1980; among individual indigobirds is that song learning Baptista 1996). In one of the best-studied estrild- is a two-stage process. Each bird in effect is guided ids, the zebra finch, Taeniopygia guttata, males through its rearing by the foster parents to the learn from their father or from other males general features of their song, then learns the depending on social conditions (e.g. Immelmann details of songs later from other firefinches or 1969; Clayton 1987a; Eales 1989; Williams 1990; from other adult indigobirds that mimic the same Slater & Mann 1991; ten Cate et al. 1993; Zann species of firefinch (Payne 1985, 1990). The strong Payne et al.: Song mimicry in a brood parasite 1539 predictions of this hypothesis are that (1) males reared by another foster species will learn the song 6 of that novel foster species and (2) males that disperse from the foster brood at the normal time of independence will copy the songs of other birds 5 that sing their foster species’ songs, including adult indigobirds that mimic these songs. An alternative hypothesis is that indigobirds have a 4 restrictive predisposition to learn the songs of their normal host species, the firefinch. The strong predictions of this hypothesis are that (1) males 3 learn firefinch song or conspecific indigobird song even after they are reared by another foster 2 species, (2) males learn firefinch songs at an earlier age than they learn other species’ songs and (3) males learn more songs of their normal host 1 species than of the alternate foster species.