The Auk 112(3):649-658, 1995

SONG MIMICRY AND ASSOCIATION OF BROOD-PARASITIC INDIGOBIRDS () WITH DYBOWSKI'S TWINSPOT (EUSTICHOSPIZA DYBOWSKII)

ROBERT B. PAYNE TMAND LAURA L. PAYNE • •Museumof Zoologyand 2Departmentof Biology,University of Michigan, Ann Arbor,Michigan 48109, USA

AI•STRACT.--Apopulation of brood-parasiticCameroon Indigobirds (Viduacamerunensis) in mimics the songsof its apparent foster ,Dybowski's Twinspot (Eusti- chospizadybowskii). Song mimicry includesthe widespreadsong elementsand phrasesand the major featuresof organizationof song(introductory units, terminal units, repetitionof certain units, and complexity in number of kinds of units in a song) of the twinspots.The songmimicry by indigobirdsof Dybowski'sTwinspots was predictedfrom a hypothesisof the origin of brood-parasiticassociations by colonizationof new foster speciesthat have parentalbehavior and habitatsimilar to their old fosterspecies. Indigobirds (Vidua spp.) now are known to mimic five speciesand generaof estrildidsthat are not (Lagonosticta spp.), their more commonfoster group. The evolutionarysignificance of songmimicry by indigobird populationsand speciesof severalgenera of estrildid finches,including the twinspot, is that the brood-parasiticindigobirds (Viduaspp.) appear to have associatedwith their fosterspecies through recentcolonizations rather than through ancientcospeciations. Received21 January1994, accepted 2 July 1994.

THE AFRICANINDIGOBIRDS (Vidua spp.) are the Viduacospeciated with them and diverged brood-parasiticfinches that often are associated at the same time in parallel with their foster with the estrildid firefinches(Lagonosticta spp.; species (Nicolai 1964, 1969, 1973). However, Nicolai 1964, 1967, 1968, Payne 1968, 1973a, other explanationsare possible.In contrastto a 1982).The adult male mimicsthe songsof the hypothesis of cospeciation,we have proposed foster species,which he learns from the foster a hypothesis of associationby colonization, species.He directs the song to the female in- when a brood parasiteswitches from one foster digobird, and not to the foster speciesitself species to another (Payne 1973a, Klein et al. (Payne 1973a, 1985). The young indigobird 1993, Payne et al. 1993). There is evidence for mimics the mouth pattern of the nestlingsof an occasionalsuccessful shift of foster species. the foster species.The breeding female visits In areaswhere two or morekinds of indigobirds the singingmale indigobird at his call-site,the live together,each usually with a different fos- place where he perchesand singson exposed ter species,a few males mimic the songsof the branches in the top of a tree, and she mates alternate foster species(Payne 1973a,Payne et with him there. In at least some areas where al. 1993). Although most kinds of indigobirds two or more kinds of indigobirdslive together, are associated with firefinches, recent fieldwork the behaveas distinct biologicalspecies; has revealed distinct populations of indigo- males and females differ in size and color from birds, some of them distinct species,that are other kinds of indigobirds, and each female associated with other kinds of estrildid finches. mateswith a male that mimics the songsof her In southern and easternAfrica, the indigobird own foster species(Payne 1973a, Payne and speciesVidua codringtoniis associatedin song Groschupf1984, Payne et al. 1993).This behav- mimicry, in distribution, and presumably in a ior may assurethat she mates with a male that, species-specificbrood-parasitic relationship with asshe did asa nestling,mimics the mouthcolors Peters'Twinspot (Hypargosniveoguttatus; Payne and patterns of the young of the same foster et al. 1992, 1993). In western , V. nigeriae species,and that their offspring also will have is associatedwith the Quail-finch (Ortygospiza this pattern. atricollis), and V. raricola is associated with the The closeassociations of indigobirdswith the Goldbreast(Amandava subfiava). Also, some pop- fosterestrildid speciesled to a suggestionthat ulations of the Indigobird (V. ca- 649 650 P^¾NE^ND P^¾NE [Auk, Vol. 112

merunensis)are associatedwith the Brown Twin- shehad laid andwas incubating. Small estrildid finches spot (Clytospizamonteiri), while others are as- of the grassand bushywoodlands of Africagenerally sociated with certain firefinches (Payne and nest late in the rains and early in the dry season Payne 1994). (Moreau 1966, Immelmann and Immelmann 1967, Our fieldwork was designedto test a predic- Payne 1973a,Elgood 1994, Payne and Payne 1994). The nest found at Freetown, Sierra Leone, had five tion of the colonization hypothesis:if the as- eggs in October (G. D. Field in litt.), and the obser- sociationsof indigobirds and their foster spe- vation of a family group in on 4 February cies are the result of colonizations of new foster (Wilkinsonet al. 1987)indicates a nestingin Decem- speciesrather than of ancientcospeciations, then ber. we expect to find additional associationsof in- CareerDonIndigobird song mimics of Dybowski's digobirds with other speciesof estrildids that Twinspotswere observedand tape recordedfrom 23 are similar in parental behavior and habitat to to 28 September 1993 within 4 km of Kabala. The the known foster species. The associationsof indigobirdswere singing from the exposedtwigs on indigobirds with two speciesof twinspots in topsof bushesand treeslocated in gardensin town, southern, eastern, and west-central Africa led as well as those locatedin cultivated fields along the roadswest towards Yagala and east towards Koina- us to searchfor songmimicry of a third species, dugu. As in other kindsof indigobirds(Payne 1973a, Dybowski's Twinspot (Eustichospizadybowskii), 1979, 1985, Payne and Payne 1994), each of the six in western Africa in Sierra Leone. males that we recorded had a set of chatters and com- plex songs(the nonmimeticsongs of the indigobird) FIELD OBSERVATIONS AND METHODS that did not resemble a foster estrildid, as well as a Dybowski'sTwinspot occurs in open grassywood- set of songs (the mimetic songs) that matched the land and grassyrock outcropsin extreme western songsof the twinspots.The malescourted the females Africa in ,, Sierra Leone, northern Li- that visited them at their call-sites.Display and be- beria and extremewestern Ivory Coast,and in west- havior were similar to the (V. chal- central Africa from Nigeria, CareerDon,Central Af- ybeata),which has been observedin detail (Payne rican Republic,, the Uelle region of Zaire, and 1973a, 1985). The indigobirds sang in the morning (Hall and Moreau 1970, Mackworth-Praed but not all day, and they fed in groups,suggesting and Grant 1973, Dowsett and Dowsett-Lemaire 1993, that Septemberwas early in their breeding season.A Matthews1995). It feedson the ground,where it takes flock of about 30 indigobirds flew from a feeding area smallgrass seeds and insects.Only onenest has been in finger millet to a mangogrove, where they roosted seenin the field in Africa (in SierraLeone; Field 1968), at dusk. One copulationwas seen. The female flew and juvenilesin a family group have been seenin to the singing male on his call-site.He hovered over Nigeria (Wilkinsonet al. 1987).It hasbeen bred by her, they matedfor 3 s, and then he flew to the ground aviculturists,and their descriptionsprovide most of andfed; she joined him. No juvenileindigobirds were what we know about its behavior. Like most estrildid seen. finches,Dybowski's Twinspot lays in well-concealed Three kinds of indigobirds are known at Kabala. covered,thatched grass nests, and both parentsre- GoldbreastIndigobirds (V. raricola)are bright glossy gurgitate seeds and occasionalinsects to their off- green; they mimic the songs of Goldbreasts.They spring,which begwith a characteristichead-twisting were tape recorded and captured at Kabala in 1973 behavior (Kunke11959, Immelmann et al. 1965, 1977a, (Payne 1976, 1982, Payne and Payne 1994);we saw Kujawa 1965,Pensold 1974, Goodwin 1982,Clewing one in 1993,but it did not sing. The other indigobirds 1988, Quoos 1990, Yantz 1991, Vit 1992). were blue, but were not captured.In September1993, Dybowski's Twinspots were observed at Kabala we recordedsix blue malesthat mimicked the songs (09ø35'N,1 Iø33'W), Koinadugu District, SierraLeone, of Dybowski'sTwinspots and six blue malesthat mim- in December 1973 and September 1993, and at icked the songsof African Firefinches (L. rubricata). Ngaoundere (07ø22'N, 13ø34'E), Tibati (06ø28'N, In December 1973, R.B.P. recorded two blue mimics 12ø38'E),and Banyo (06ø45'N,IIø50'E) in northern of thisfirefinch (Payne 1976). All of the singingmale CareerDonin January1979 and October1980 and 1992. blue indigobirds(both twinspot mimicsand At Kabala,the rainy seasonis from May throughOc- mimics)appeared to have the samecolor and intensity tober,with eachmonth averagingmore than I00 mm of glossin breedingplumage, and the samepale wings of rainfall (Gwynne-Joneset al. 1978).By December and pale purplish feet; it is on this basisthat we the grassis dry and the hillsidesare burned(Payne identifiedthem as V. camerunensis(cf.Payne and Payne 1976).In Septemberthe twinspotsfed on fallen grass 1994). Goldbreasts and African Fire finches were seen seeds,especially finger millet ("funde") in cultivated there with Dybowski'sTwinspots. The other estril- fieldswhere the smallseeds were being harvested.A dids at Kabalaknown as fosterspecies of certain in- female netted on 26 September1993 was in fresh digobirds (Payne 1976, 1982,Payne and Payne 1994) plumageand hadfour recently-ovulatedovarian fol- were the Red-billedFirefinch (L. senegala),Bar-breast- liclesand an edematousbrood patch, indicating that ed Firefinch(L. rufopicta),and Black-belliedFirefinch July1995] IndigobirdsMimic Twinspot Songs 651

(L. rara). No indigobirds were found there with the The songsand callsof the Dybowski'sTwin- songsof these finches. spotshave a variety of units. Some of these Songswere recordedin the field with a SonyTC- intergrade,and additionalrecordings may show D5M cassette recorder or Uher 5000-series recorder moreintermediates. The following elements and and a SennheiserME-40 microphonein a parabolic reflector.The numberof songsrecorded varied among phrasesare apparentin our recordedsamples malesand ranged from 20 to more than 600. Also, a of a twinspotpair and their two grown sons familyof Dybowski'sTwinspots of unknowncountry that they rearedin captivity,and of a wild male of origin were observedin captivity,with morethan in the field at Banyo, Cameroon.The 11 ele- 50songs recorded for eachof threemales and 20 songs ments (where a single trace is involved) and for the female.Audiospectrograms were madewith phrases(where more than one element makes a Kay ElemetricsDSP Sona-Graph 5000 at transform up a repeatingunit) of songare labelledin Fig- sizeof 256 pts (234Hz) and a Krohn-Hiteband-pass ure 1 and are described below: (1) The alarm filter model310-AB with low passat 1.4kHz to sup- call is a short (0.02-s)element of a rising fre- presslow-frequency background noise. quency with two distinct tracings. The call soundslike "zit" and correspondsto the "zit" RESULTS calls of Immelmann et al. (1965) and Kujawa (1965), and the "tsit" or "tset" call of Goodwin Callsand songs of Dybowski'sTwinspots.--Vocal (1982).In captivesthe call is given repeatedly behavior of the twinspot has been described when the is disturbed. The number of times with transliterationsand comparedwith Eu- "zit" is repeatedvaries considerably;it some- ropean ,but without audiospectro- times is given alone and sometimesin series of grams. Goodwin (1982) noted that: 10 or more, and usually not in threes ("zit-zit- zit") asin Immelmannet al. (1965)and Kujawa The alarm call is a loud 'tset-tset-tset' or 'tsit-tsit- (1965).(2) A contactcall "kek" is tracedby an tsit.' A softer, run-together'tsit-tsit' may be a close inverted V-shape,and it often has a harmonic contactor locomotionintention call. The songof the overtone. It is given by a bird separatedfrom maleis complexand variable.Individuals vary their its mate.This maybe the "zet" of Kujawa(1965) songsand there is considerablevariation betweenthe and Goodwin (1982). (3) An element "r" often song repertoire of individuals. The same bird in its is given in seriesin a trill, and "r-r-r..." varies songcommonly produces phrases suggestive of the rolling trill of a Canary[Serinus canarius], the deep amongseries from 0.03 to 0.1 s in duration and notesof the Nightingale [Lusciniamegarhynchos] and descendsin frequency. The trilled phrase is the fluting phrasesof the Blackbird,Turdus merula, similarto the trill or tourof a Canary(G/ittinger song. Song is given when alone, most often when 1979,1981, 1985). This may be the "r-r-r" of the perchedin cover,and in display.The female also twinspot song in Immelmann et al. (1965). (4) sings,especially if unpairedand alone, her songis An element "t" is given in a trill, "t-t-t" and softer than but otherwise like the male's. may be a short "zit"; it has a duration of 0.02 to 0.05s and ascendsin frequency.This may be Kujawa (1965) described the contact call the "t-t" describedby Immelmannet al. (1965). ("Lockruf") as a string of "zit-zit," which in (5) A "tu" is a whistledelement, rising then excitement change into a sharp, quick three- falling in frequency,and brief in duration(< 0.1 syllable "zit-zit-zit." Another contact call is a "zschip-zschip."Immelmann et al. (1965) de- s). It oftenis given in seriesin a harshemphatic scribedthe excitementcall ("Erregungsruf")as trill, similar to a Canarytour (G•ttinger 1981, 1985). Variants of "tu" include: "teu," which is a sharp, quick three-syllable "zit zit zit." The song of the male is fluctuating and versatile. broader,rising then falling, and often with a Kujawa (in Immelmann et al. 1965) transcribed strongharmonic band that givesa shortwheezy the song as "w/i-/i- t/i- t/i- t- r- r- r- r- r- t __ sound; "tix," which rises then has a double, w/i- w/i- tia- w/lit- t- r- r- r- r- r- tsit- sit __ sit." inverted U-shapewhistle at about 6.4 kHz; "ru," The "t" and "r" soundsare like the rolling trill which is a descendingcall intermediate in shape of Canaries,while the intermediatefollowing between "teu" and the shorter "r"; and "chink," tonesare similar to the guttural soundsof the which is a whistle with a sharp rise at the end, Nightingale. The singing male staysin dense sometimesgiven in a series of elements that vegetationabout 0.5 m abovethe ground. Im- intergradewith "tu." (6) A buzzyphrase "churr" reelmann et al. (1977a) noted that the male has is a rapidly amplitude-modulatedphrase with severalclear loud songswith variations. mostenergy at 4 to 5 kHz and a periodicity of 652 PAYNEAND PAYNE [Auk, Vol. 112

Eustichospizadybowskii Dybowski's Twinspot

t-t.... zitzit -weee • churr • • chu•r- vwoee

d zi•t• sitt-t-t

l•zlt zit.... '.... leo-- r-r-r' ' toto chink. ix,- churr --L - : - - -: -_ ."- •L '•---._-"_7 ...... -._• .... .-

•it • t-t-t ru • i• ru k•k k•k

ß . • • ' 101h _ _ _ j _ j •-I..... • .... I• h.,•., ,...,.,.•_...... __•._-..... ].•!•!h

kHz 1.0 • Fig. I. Songso[ Dybowski'sTwinspot: (a-e) captivemale t63; (I-g) captive[emale (mother o[ t63);(h-j) songso[ wild maleat Banyo,Cameroon, recorded on 9 NovemberI980 (with singinginsect at 4-5 kHz). TtansHtetationscorrespond in part to descriptionso[ songo[ twinspot(ImmeIman• et aI. I965, KujawaI965, GoodwinI982) andother songbirds, espedaIIy Nightingales and Blackbirds (Bergmann and Heib I982, Roch6 I986, Crop I988).

0.01 s, "Churr" often is introduced by a short "Weee" is a whistle that ascendsin frequency descendingelement. (7) A buzzy phrase"churr" and varies in form (inflected or simple) and combined with an overtone at 6 kHz that duration (0.05 to 0.3 s). These intergrade with changesin tonal quality into a whistle, pro- the short whistle "tu." (10) "Vweee" is a whistle ducesa sound"vwurrr." (8) A "sit" phrasecom- with two or three strongharmonic bands in the bines two short slurred whistles that are pro- rangeof 3 to 8 kHz. Thesehave a wheezy,ka- duced simultaneously,the higher part ascend- zoolike tonal quality and are one of the most ing from 5.6 to 6.4 kHz, while the lower ascends distinctive soundsof twinspot song. (11) "Wee- from 4 to 6 kHz, or two tones in which the lower zu" is an inflected whistle that changesfrom 6 one ascends,while the upper one descends.The to 3 kHz and has a marked inflection in fre- simultaneousproduction of two soundswith quency. The male twinspot at Banyo had it. tracingshaving no simple relationship,such as The songsof Dybowski'sTwinspots combine overtones, in the structure of the bands that rise several kinds of elements and phrasesin a pat- and fall out of parallel ("sit," "vwurrr") may be tern with someconsistency from one rendition due to the two sidesof the syrinx (Greenewalt to the next. The songs include the following 1968). Both males and females gave "sit." (9) general featuresof syntax and order: (1) The July1995] IndigobirdsMimic Twinspot Songs 653

Viduacamerunensis Twinspot Indigobird

sit t-t-t teu zitzit tu tu chuff chooc ru •_ ,, •-- •N•oc ' _•_[_•_• ...... d.,h Ird J • ....

.... tix • _•ging call sit t-t-t teozJt ! tu churrCb•o c

2 - kHz, , , , , 1•.0s Fig. 2. Songsof adult male indigobirds(Vidua camerunensis) at Kabala, Sierra Leone: (a-f) male t2, 2 km eastof Kabala,recorded on 24 September1993; (g) male tl, 1 km westof Kabala,recorded on 23 September 1993.Note resemblanceof songelements, phrases, and songstructure to thoseof Dybowski'sTwinspots in Figure1, and similarityof songswithin and betweentwo maleindigobirds, tl and t2. song is introduced by an alarm note "zit." (2) of trills that are introducedwith single sharp A "sit" phrase occursearly in the song se- notesand interspersedwith churrs,kazoos, and quence.(3) A trilled phrase "r-r-r," "t-t-t," or whistles that rise or fall in pitch. Immelmann "tu-tu" is repeatedwith the numberof elements et al. (1977a)suggested that femaleshave a sin- in a phraseinversely related to the period from gle song. Our captive female had short, soft onset of one element to the next, and to the songs(Fig. lf, g), with simpler elements,lack- duration of the element. This phrase corre- ing rapid trills, and with longer duration be- spondsto the Canarylikeroiling trill noted for tween the elements(males sometimes sang like a song of the twinspot by Immelmann et al. this; Fig. la). She had three or four versionsof (1965).(4) A buzzy"churr" or "vwurr" is given songthat were aboutas consistentas the song singly. (5) Song often ends with a whistle or typesof the males.The wild male in Banyohad seriesof whistles,a rising or falling "tu," "teu," songs similar to those of captive males, al- or "ru," or an ascending"weee" or wheezy though the songsdiffered in detail (Fig. lh-j), "vweee." "Choocchooc" also appears near the suggesting that the captives originated else- end of song.The constantfeatures of songor- where. ganization,as well as the elementsand phrases Songmimicry by indigobirds.--Mostcalls and that are widespreadin the species'songs, may song elementsrecorded in the twinspotsalso be species-universalfeatures of behavior (Mar- were given by the indigobirdsat Kabala (Fig. ler and Nelson 1992). 2), including the following: (1) Mimetic "zit- Eachcaptive male twinspot had three or more zit" elementsare given in seriesof this element songswith differentcombinations and ordering and in repeated,nearly stereotypedsequences of elements. Each version varied with substi- of different elementsand phrasesof mimicry tutions and deletions or insertions of elements song.(2) Mimetic"kek" elements are given alone and sequences(Fig. la-e). The songsof the three and may be given in stereotypedsequences in males were similar, but differed in the details the song.(3, 4) Trilled seriesof "t-t-t" are given of the shape of the elements and phrases,and in repeated mimicry songs.The "r" elements in their sequence.The overall impressionof a are representedas whistled descending"ru"; twinspotsong is of a rapidly deliveredsequence some have an introductory"t" as in "teu" or 654 PAYNEa•qD PAYNE [Auk,Vol. 112

"kek." (5) Whistledseries of "tu" aregiven both the songsof twinspots.Upon hearing the in- aloneand in trills in the complexmimicry songs. digobirdsin the field, we recognizedat once Variants "teu," "ru," and "tix" also are given that they matched the songs of Dybowski's in mimicry songs.(6, 7) The "churr" phrases Twinspots. are matchedby the indigobirdswith a period- Eachindigobird at Kabalamatched the mim- icity of about 0.01 s, as in the twinspot "churr" icry songsof the neighboringmale indigobirds and "vwurr." (8) A two-part "sit" occursin the with the samesequence of elementsand phras- mimicry songsof the indigobird. (9, I0) As- es (Fig. 2e, g). The neighboringmales differed cendingwhistles "weee" intergraded with "teu" among themselvesmainly in the number of and were long as in the song of a female twin- short elements("zit") that were repeatedin a spot.The longest"weee" in the indigobirdswas series and in the form of whistled "teu" ele- a wheezy whistle with a wavering kazoolike ments;these differences appeared to be consis- tonal quality and amplitude modulation as in tent. the twinspot "vweee." A version"chooc chooc" In additionto the mimicrysongs, which com- is a compound "weee" or "vweee" with two prisedabout 20% of their songs,the indigobirds ascendingelements. The phraseis like "chooc" alsohad a set of nonmimeticsongs shared by of Nightingale (Roch• 1986,Cramp 1988)and all six malesrecorded in the population.These is similar to the twinspot "weee" or "vwee" were composedof differentsong elements and with a short clink as in the twinspot "chink" phrases,most of them harshin sound,though (Fig. I). (12) In addition to mimicry of the twin- a few weresimilar to elementsin twinspotsongs spotadult calls,song elements, and songphras- and may be modified from them. Much as in es, a series of elements like "tix" formed a another indigobird species, the nonmimetic rhythmic phrasethat resembles"begging" of songs are modified from elements of the mi- nestlings and juveniles of certain estrildid metic songsthrough cultural evolution (Payne finches(Payne 1973a,Payne and Payne 1994). 1973a, 1985). The seriesappears to be a mimeticbegging call given by the adult indigobirds.We have not DISCUSSION recordedthe callsof beggingyoung Dybowski's Twinspots. The songsof six adult indigobirdsin Sierra Nearly all elements and phrasesthat we re- Leonematched the callsand songsof Dybow- cordedin the songsof Dybowski'sTwinspots ski'sTwinspot. Nearly all elementsand phrases were identifiedin the songsof indigobirds(Figs. identified in the vocal repertoiresof the twin- 1 and 2). The units of twinspotsongs may vary spotswere identified in the indigobirdsas well. from region to region, and we did not record Also, the majorfeatures of songorganization the twinspotsat Kabala. Twinspot songsthat were featuredby the indigobirds.The indigo- we heard there had sharp"kek-kek" elements, birds appear to match the "species-universal" emphatic"tu-tu" trills, and wheezy kazoowhis- featuresof songof the twinspots,as well ashave tles "teu" and "vweee." These were heard and their own nonmimeticsong repertoire. recordedin the mimetic songsof indigobirds. The songmimicry indicatesthat a population The complex songs of the indigobirds that of indigobirds is a brood parasiteof the twin- had songelements and phraseslike thoseof the spot,although direct field evidenceof its brood twinspot were organizedin a sequencesimilar parasitismremains to be determined.The mim- to that found in twinspotsongs: (I) songswere icry songspresumably are learnednot only from introduced by a short "zit" element; (2) "sit" the twinspotsas fosterspecies, but alsolater by followed "zit"; (3) short elements particularly the adult male from other male indigobirdsthat the whistled "tu-tu" and "chooc-chooc" were mimic the same speciesof twinspot. Much as repeatedin series;(4) long modulatedphrases in Village Indigobirds, the indigobirds learn "churr" were given singly; and (5) songoften their songsboth from their fosterspecies, the ended with one to three whistles, a "vweee," Red-billed Firefinch, and from each other. Both "ru," "teu," or "chooc chooc" series. The com- individually marked male indigobirdsrecorded plexity and major featuresof organization of from seasonto seasonin the field and captive mimicry songs (introductory units, terminal malesmodified the songof their fosterspecies units, repetition of certain units, and number and copied each others' song variants, as well of kinds of units in a song)all were similar to asthe songsof individualsof the fosterspecies, July1995] IndigobirdsMimic Twinspot Songs 655 even when thesewere not their own fosterpar- Although some speciesof estrildids have dif- ents (Payne 1985, 1990). ferent calls in malesand females(Payne 1982, There are severalexplanations for the vari- Zann 1984,Yoneda and Okanoya 1991), in some ations observedin songsof the song models the females have songs that are shorter than and song mimicry (Figs. ! and 2). These point thoseof the males(Gahr and Giittinger 1986), out some important features of song mimicry and some indigobirds mimic the vocalizations in indigobirds,including: songvariation among of femalesof their foster species,as well as the individual twinspots;sexual strategies in male calls and songsof males (Payne 1982). None of indigobirds; variation among populations of the mimicry songsof the Kabala indigobirds twinspots (much as in other speciesof estril- could be determined as femalelike rather than dids, Payne 1973a,b, 1985);and improvisation malelike. We have no information on the geo- and cultural drift on song theme of the foster graphic variation in the songsof Dybowski's species.First, the variationsin songswithin and Twinspots,but other speciesof fosterestrildids among twinspots appear to be as great as the are known to vary geographicallyin their songs variations in songs of indigobirds; song varia- (Payne 1973a,b, 1990),and it is possiblethat tion in twinspotsmay accountfor the variation the differencesbetween the songsof the indi- observed in songs of the indigobird. A male gobirds and the captive twinspots are based in indigobird has three song types like those of a different geographicorigin. twinspots.Our observationthat a male twinspot The mimetic songsof the indigobirds in Si- also has three or more songs does not neces- erra Leone were more like thoseof Dybowski's sarily indicatethat the male indigobird recalls Twinspotsthan were the songsof indigobirds and matchesthe details of songsof his foster that mimicked Brown Twinspots in Cameroon father, given the knowledgethat a male in an- (Payne and Payne 1994). The variation in the other speciesof indigobird has three or four match to a foster speciesmay indicate a course nonmimeticsongs that mimic his fosterspecies, of cultural evolution through drift in song, while in his fosterspecies a male hasonly one where a maleindigobird mimics the songof the or two song types (Payne 1973a, 1985, 1990). foster speciesand then his year to year impro- This variation in the mimicry songsof a male visationson the song theme accumulate,until indigobirdis thoughtto be a sexually-selected the songtheme is no longer recognizableas a behavior enabling males to attract more fe- mimicrysong. Other male indigobirdscopy the males;different femaleshave been reared by songvariants of a successfulbreeding indigo- fosterparents with different songs,so any one bird into a populationwidesong theme (Payne of their songsmay be like one of the male in- 1985).Finally, in spite of thesesources of vari- digobird's mimicry songs if he has a mimetic ation in songsof model and mimic, we point repertoirerather than only a single mimicry out that the indigobird mimics of Dybowski's song.The polygynousmating systemof the in- Twinspots sang songs that were as precise a digobirds (Payne and Payne 1977) appearsto matchto the songsof Dybowski'sTwinspots as selectfor a repertoireof songmimicry, and not are the songs known for any speciesof indi- just for mimicry of a single song of the foster gobirdwith its fosterspecies (Payne 1973a, 1982, species(Payne 1983, 1990). As in other species Payne and Payne 1994). of indigobirds, the six indigobird males that The speciesstatus of the indigobirdsassoci- mimicked the songsof Dybowski'sTwinspots ated with Dybowski's Twinspots is uncertain. at Kabalaalso shared their mimicrysongs among Becausethe mimicry songsare learned (Payne themselves.It is unlikely that all had the same 1985)and the plumageof theseadult indigo- fosterfather, and it is likely that they learned birds is not known to be distinctive, the evi- from each other, or rather from the same in- dencethat would allow the birds to be recog- dividual male indigobird source,as in other in- nized as a distinct speciesis not available. One digobirds (Payne 1985). Twinspots were more genetic diagnostic of a viduine speciesis the abundant than indigobirds at Kabala. Where appearanceof its young. Dybowski'sTwinspot populationdensities were determinedin recap- nestlingsand fledgedyoung have a whitishgape tures of color-marked birds and in transect cen- andmouth lining, thepalate has five blackspots, suses in , the Red-billed Fire finch was a pair of black spotsline the inside of the white 10times more numerous than its brood parasite, oral flange, and the floor of the mouth has a the Village Indigobird(Payne and Payne1977). black crescent(Kujawa 1965, Immelmann et al. 656 PA¾•qEANt) PA¾•qE [Auk, Vol. 112

1977a).The mouth pattern is like that of Brown with the socialand feeding conditions.Immel-. Twinspotsand Peters' Twinspots, except in those mann et al. (1977b) comparedthe growth of speciesthe palate and oral flange are yellow nestling Zebra Finches (Taeniopygiaguttata) (Goodwin 1982). The mouth pattern of the having normally-pigmentedmouth markings youngindigobirds associated with Dybowski's with white morphsthat lackedthese markings. Twinspotsis unknown, as are the mouth pat- Wild-colorednestlings were given more food, terns of someother mimicry song populations had priority to first feedingsof the day, grew of indigobirds(including some in which adults faster,and had higher survival.Both adult white- are morphologicallydistinct; Payne et al. 1992). plumagedand adult wild-color Zebra Finches Indigobirdsknown by their breedingplumage fed preferentially the wild-pattern young in a asV. camerunensisinclude mimicsof Dybowski's mixed brood. Nevertheless, the successof nest- Twinspots, Brown Twinspots, Black-bellied lings with odd mouth patterns appearsto vary Firefinches, and African Firefinches(Payne and with environmental conditions. Both Skagen Payne1994). The mouthpatterns of the young (1988) and Reed and Freeman(1991) compared finchesdiffer amongthese four presumedfoster normal and unmarked nestlings in conditions species(Immelmann et al. 1965,Payne 1982). where the foodsupply was varied. Skagen (1988) The only juvenile indigobird that wascaptured found a differential rate of growth, with the from thesepopulations matched the mouthpat- unmarked young growing more slowly when tern of the Black-belliedFire finch (Payne and food was limited, but no difference when food Payne1994), and it is unknownwhether all the was abundant; in neither condition was there correspondingindigobirds have genetic adap- a difference in survival to fledging. Reed and tations that mimic their foster species'young. Freeman (1991) found a differential survival of If they do, then perhapsthe indigobird mimics young,with the usualmouth pattern doing bet- of Dybowski'sTwinspot are a distinctspecies. ter than unmarked young in experimentalcon- However, the population that mimics the ditions of limited food, but equal survival in songsof the twinspotmay have a shorthistory conditionsof plenty. The results of these ex- of associationwith that species.It may have perimentsin a nestingestrildid suggest the con- switchedfrom one foster species(perhaps the ditions needed for a young brood parasiticvi- widespreadAfrican Firefinch)to a new foster duine finch to survive in the nest of a species species,and it maynot yet havebeen selected whose own young have a different mouth pat- for geneticadaptations of its youngto match tern. the mouthpattern and colorsof the youngtwin- The occurrenceof a population of indigo- spot.Survival with an alternatefoster species birds associatedwith Dybowski'sTwinspot was in the indigobirdsis possible,and there is field predicted from the occurrenceof other kinds evidence of such switches at least at the indi- of indigobirdsthat mimic two other speciesof vidual level. Occasionally,male indigobirds(1% twinspots(Payne et al. 1992, Payne and Payne of 484 malesin areaswhere two or more species 1993), and from the similarity in parental be- of indigobirdslive togetherin southernand havior and habitatof Dybowski'sTwinspot with eastern Africa) have been recorded with songs thoseof the firefinchesand the other twinspot mimickinga speciesof estrildidthat is not their species.In fact,we predictedthis associationto usualfoster species (Payne 1973a,Payne et al. colleaguesat a scientific meeting during the 1993), and their unusual song mimicry suggests month before we did the fieldwork in Sierra that theywere rearedby an alternatefoster spe- Leone.The songmimicry of indigobirdson Dy- cies of estrildid finch, and not by their usual bowski'sTwinspot providessupport for the hy- fosterspecies. Although the indigobirdnest- pothesisthat the indigobirds have associated lingsthat hatchin the nestof an unusualfoster with many speciesof estrildid fostersthrough speciesare sometimesdisadvantaged in receiv- a processof colonization rather than ancient ing parentalcare from their fosterparents, we cospeciation.The twinspots,the Goldbreast,and suspectthat in someconditions mouth mimicry the Quail-finch are not thought to be closely of their fosterspecies' nestlings is not necessary related to the fire finches or to each other, and for them to survive to fledging and indepen- there is somequestion about the monophyly of dence. the twinspots(Kakizawa and Watada1985, Wol- Survivalof the youngbrood parasites in the ters 1987);however, the indigobirdsare closely brood of an alternate foster species may vary related to eachother. Also, their fosterspecies' July1995] IndigobirdsMimic Twinspot Songs 657 clades, as perceived by Kakizawa and Watada GOTlINGER,H.R. 1981. Self-differentiation of song (1985) and Wolters (1987), include other estril- organizationrules by deaf Canaries.Z. Tierpsy- did species--Violet-eared Waxbill ( chol. 56:323-340. granatina)and (G. ianthinogas- GOTTINGER,H. R. 1985. Consequencesof domesti- cation on the song structuresin the Canary. Be- ter)--that are parasitizedby other speciesgroups haviour 94:254-278. of viduine finches (Nicolai 1964, 1973). Both GWYNNE-JoN•S,D. R. G., P. K. MrrCH•L, M. E. HARV•, molecular and morphological evidence suggest AND K. SWINDELL.1978. A new geography of that the indigobird brood parasiteshave colo- Sierra Leone. Longman, London. nized their foster specieswell after the foster HALL, B. P., AND R. E. MOREAU. 1970. An atlas of species had diverged, rather than having co- speciationin African passerincbirds. British Mu- speciatedalong with them (Payne 1973a,Klein seum(Natural History), London. et al. 1993, Payne et al. 1993). IMMELMANN, K., AND G. IMMELMANN. 1967. Verhal- tensiSkologischeStudien an afrikanischen und australischenEstrildiden. Zool. Jb. Syst. Bd. 94: 609-686. ACKNOWLEDGMENTS IMMECMANN,K., J. STEINS^CHER,AND H. E. WOLT•RS. H. Thompsonhelped with arrangements,and the 1965. Prachtfinken, 2nd ed. Vol. 1, Astrilde. Ver- Ministry of Agriculture, Natural Resourcesand For- lag Hans Limberg,Aachen, Germany. estryprovided permits for scientificresearch in Sierra IMMELMANN,K., J. STEINSACHER,AND H. E. WOLTERS. Leone.L. F. Baptistamade availablethe captiveDy- 1977a. Prachtfinken, 2nd ed. Vol. 2, Amadinen. bowski'sTwinspots. L. F. Baptista,G. D. Field, G. D. Verlag Hans Limberg,Aachen, Germany. Schnell, J. L. Woods, and T. Yuri commented on the IMMELMANN, K., A. Pr•TZ, AND R. SOSSINKA. 1977b. manuscript.Fieldwork was supportedin part by the ExperimentelleUntersuchungen zur Bedeutung NationalScience Foundation and National Geograph- der Rachenzeichnungenjunger Zebrafinken.Z. ic Society. Tierpsychol.45:210-218. KAKIZAwA, R., AND M. WATADA. 1985. The evolu- tionary genetics of the . J. Yamashina LnmP,a•R• CITED Inst. Ornithol. 17:143-158. KLEIN, N. K., R. B. PAYNE, AND M. E. D. NHLANE. 1993. BERGMANN,H.-H., AND H.-W. HELS. 1982. Sftmmen A moleculargenetic perspective on speciationin der Vi3gel Europas. BLV Verlagsgesellschaft, the broodparasitic Vidua finches. Proc. VIII Pan- Mfinchen. AfricanOrnithol. Congress, Bujumbura, 1992:29- CLEWING,T. 1988. Haltung und Zucht des Dybow- 39. skisTropfenastrild Eustichospiza dybowskii Oustal- KUJAWA,W. 1965. Die Erstzuchtdes Dybowskis et, 1892. Gefiederte Welt 112:14-15. TropfenastrildEustichospiza dybowskii (Oust.). Ge- CRAMP,S. (Ed.). 1988. The birds of the western Pa- fiederte Welt 1965:222-225. learcftc, vol. 5. Oxford Univ. Press, Oxford. KUNKEL,P. 1959. Zum Verhalten einiger Prachtfin- Dowsm'r, R. J., AND F. DOWSm'r-LEMAn•(EDS.). 1993. ken (Estrildinae).Z. Tierpsychol.16:302-350. A contributionto the distribution and MACKWORTH-PRAED,C. W., AND C. H. B. GRANT. 1973. of Afrotropicaland Malagasybirds. Tauraco Res. Birds of west central and western Africa, vol. 2. Rep. 5. Longman, London. ELGOOD,J. 1994. The birds of Nigeria. Check-listno. MARLER, P., AND D. NELSON. 1992. Neuroselection 4, 2nd ed. British OrnithologistsUnion, London. and songlearning in birds:Species universals in FIELD, G.D. 1968. Birds of the Freetown area. Fourah a culturally transmitted behavior. Semin. Neu- BayCollege Bookshop, Freetown, Sierra Leone. rosci. 4:415-423. GAHR, M., AND H. R. GO•nNGER. 1986. Functional M^TTHmVS,R. 1995. Uganda ForestBiodiversity In- aspectsof singingin male and female ventory Programme. Bull. Aft. Bird Club 2:6. bengalus(Estrildidae). Ethology 72:123-131. MOREAU, R. E. 1966. The bird faunas of Africa and GOODWIN, D. 1982. Estrildid finches of the world. its islands. Academic Press, New York. British Museum (Natural History), London. NICOLm,J. 1964. Der Brutparasitismusder Viduinae GREENEWALT,C.H. 1968. Bird song: Acousticsand alsethologisches Problem. Z. Tierpsychol.21:129- physiology. Smithsonian Institution Press, 204. Washington,D.C. NICOLm,J. 1967. Rassen-und Artbildung in der Vi- GOTT•NGER,H.R. 1979. The integrationof learnt and duinengattungHypochera. 1. Hypocherapurpur- geneticallyprogrammed behaviour: A study of ascensReichenow--Brutparasit beim Dunkelto- hierarchial organization in songs of Canaries, ten Amaranten Lagonostictarubricata (Lichten- Greenfinchesand their hybrids.Z. Tierpsychol. stein). J. Ornithol. 108:309-319. 49:285-303. NICOLAI,J. 1968. Wirtsvogel-Beziehungender Hy- 658 PAYNEAND PAYNE [Auk, Vol. 112

pocheraFormen camerunensisund nigeriae.Natur- PAYNE,R. B., AND K. PAYNE. 1977. Socialorganiza- wiss. 53:654. tion and matingsuccess in localsong populations NICOLAI,J. 1969. BeobachtungenanParadieswitwen of Village Indigobirds,Vidua chalybeata. Z. Tier- (Steganuraparadisaea L., Steganuraobtusa Chapin) psychol.45:113-173. und der Strohwitwe(Tetraenura fischeri Reichen- PAYNE,R. B., ANDL. L. PAYNE. 1994. Song mimicry ow) in Ostafrika. J. Ornithol. 110:421-447. and speciesstatus of the indigobirds Vidua:As- NICOLA/, J. 1973. Das Lernprogramm in der Ge- sociationswith Quail-finch Ortygospizaatricollis, sangsausbildungder Strohwitwe Tetraenurafis- GoldbreastAmandava subfiava and Brown Twin- cheriReichenow. Z. Tierpsychol. 32:113-138. spot Clytospizamonteiri. Ibis 136:291-304. PAYNE,R.B. 1968. Mimicry and relationshipsin the PAYNE, R. B., L. L. PAYNE, •ND M.E. D. NHLANE. 1992. indigobirdsor combassousof Nigeria. Nigerian Song mimicry and speciesstatus of the Green Ornithol. Soc. Bull. 5:57-60. Widowfinch Viduacodringtoni. Ostrich 63:86-97. PAYNE,R. B. 1973a. Behavior, mimetic songs and PAYNE, R. B., L. L. PAYNE, M.E. D. Nh--t•NE, AND K. song dialects,and relationshipsof the parasitic HUSTLER.1993. Speciesstatus and distribution indigobirds(Vidua) of Africa. Ornithol. Monogr. of the parasitic indigo-birds Vidua in east and 11. southern Africa. Proc. VIII Pan-Aft. Ornithol. PAYNE,R. B. 1973b. Vocal mimicry of the paradise Congr.:40-52. whydabs(Vidua) and responseof female whyd- PENSOLD,R. 1974. Beobachtungenbei der Haltung absto the songsof their hosts(Pytilia) and their und Zucht des Dybowskys Tropfenastrild. Ge- mimics. Anim. Behav. 21:762-771. fiederte Welt 98:109-110. PAYNE,R. B. 1976. Song mimicry and speciesrela- Quoos, D. 1990. Teufel mit Charme--Dybowskis tionshipsamong the West African pale-winged TropfenastrildEustichospiza dybowskii (Oust.). Ge- indigobirds.Auk 93:25-38. fiederte Welt 114:301-303. PAYNE,R. B. 1979. Song structure, behaviour, and REED, H. J., AND N.H. FREEMAN. 1991. Does an ab- sequenceof songtypes in a populationof Village senceof gapemarkings affect survival of leucistic Indigobirds, Vidua chalybeata.Anim. Behav. 27: young in the Zebra Finch?Bird Behav.9:58-63. 997-1013. RocI-I/•,J.C. 1986. Die VogelstimmenEuropas. Ton- PAYNE,R. B. 1982. Specieslimits in the indigobirds band-Cassetten. Kosmos WB-ALL-3K7-86, Stutt- (Ploceidae, Vidua) of West Africa: Mouth mim- gart, Germany. icry, songmimicry, and descriptionof new spe- SKAte, S.K. 1988. Asynchronoushatching and food cies. Misc. Publ. Univ. Mich. Mus. Zool. 162. limitation: A test of Lack'shypothesis. Auk 105: PAYNE,R.B. 1983. Bird songs,sexual selection,and 78-88. female mating strategies.Pages 55-90 in Social Vrr, R. 1992. Erfahrungenmit DybowskisTropfen- behavior of female vertebrates (S. K. Wasset, Ed.). astrilden. Gefiederte Welt 116:274-276. Academic Press, New York. WILKINSON, R., R. BEECROFT,A. U. EZEALOR,AND R. E. PAYNE,R. B. 1985. Behavioralcontinuity and change SHAlt,AND. 1987. Dybowski's Twinspots in the in localsong populations of Village Indigobirds Kagoro Hills, Nigeria. Malimbus 9:134. Viduachalybeata. Z. Tierpsychol.70:1-44. WOLTERS,H. E. 1987. Zur Stammesgeschichteder PAYNE,R.B. 1990. Songmimicry by the Village In- afrikanischen Prachtfinken. Trochilus 8:46-60. digobird(Vidua chalybeata) of the Red-billedFire- YANTZ, J. 1991. Dybowski's Twinspot. Am. Cage- finch (Lagonostictasenegala). Vogelwarte 35:321- Bird Mag. 63(8):65-75. 328. YONEDA,T., AND OKANOYA,K. 1991. Ontogeny of PAYNE, R. B., AND K. D. GROSCHUPF. 1984. Sexual sexually dimorphic distance calls in Bengalese selection and interspecificcompetition: A field Finches (Lonchuradomestica). J. Ethol. 9:41-46. experiment on territorial behavior of nonpar- ZANN, R.A. 1984. Structural variations in the Zebra ental finches (Vidua spp.). Auk 101:140-145. Finch distancecall. Z. Tierpsychol.66:328-345.