Three-Wattled Bellbird–2013 Wilson Journal
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Published by the Wilson Ornithological Society VOL. 125, NO. 1 March 2013 PAGES 1–232 The Wilson Journal of Ornithology 125(1):1–14, 2013 BEHAVIORAL EVIDENCE FOR SONG LEARNING IN THE SUBOSCINE BELLBIRDS (PROCNIAS SPP.; COTINGIDAE) DONALD KROODSMA,1,9 DEBRA HAMILTON,2 JULIO E. SA´ NCHEZ,3 BRUCE E. BYERS,4 HERNA´ N FANDIN˜ O-MARIN˜ O,5 DAVID W. STEMPLE,6 JILL M. TRAINER,7 AND GEORGE V. N. POWELL8 ABSTRACT.—Why vocal learning has evolved in songbirds, parrots, and hummingbirds but not in other avian groups remains an unanswered question. The difficulty in providing an answer stems not only from the challenge of reconstructing the conditions that favored vocal learning among ancestors of these groups but also from our incomplete knowledge of extant birds. Here we provide multiple lines of evidence for a previously undocumented, evolutionarily independent origin of vocal learning among the suboscine passerines. Working with bellbirds (Procnias spp.), we show that (1) a captive- reared Bare-throated Bellbird (P. nudicollis) deprived of conspecific song not only developed abnormal conspecific songs but also learned the calls of a Chopi Blackbird (Gnorimopsar chopi) near which it was housed; (2) songs of Three-wattled Bellbirds (P. tricarunculata) occur in three geographically distinct dialects (from north to south: Nicaragua, Monteverde, and Talamanca); (3) Three-wattled Bellbirds at Monteverde, Costa Rica, are often bilingual, having learned the complete song repertoire of both the Monteverde and Talamanca dialects; (4) immature bellbirds have an extended period of song development, lasting the 6 years in which they are in subadult plumage; and (5) adult male Three-wattled Bellbirds continually relearn their songs, visiting each others’ song perches and adjusting their songs to track population-wide changes. Perhaps female preferences and strong sexual selection have favored vocal learning among bellbirds, and additional surveys for vocal learning among other lekking cotingas and other suboscines may reveal patterns that help determine the conditions that promote the evolution of vocal learning. Received 21 February 2012. Accepted 13 July 2012. Key words: bellbird, birdsong, Contingidae, dialects, evolution, Procnias, vocal learning. 1 52 School Sreet, Hatfield, MA 01038, USA. One of the most frequently asked but unan- 2 Fundacion Conservacionista Costarricense, Monte- swered questions among those who study bird- verde, Puntarenas, Costa Rica. song, is why vocal learning evolved among 3 Unio´n de Ornito´logos de Costa Rica, Apdo 11695-1000, parrots, hummingbirds, and passerines but not San Jose´, Costa Rica. 4 other species groups, and within the passerines Department of Biology, University of Massachusetts, why in oscine songbirds but not in their sister Amherst, MA 01003, USA. 5 Departamento de Biologia Animal e Vegetal, Universi- group the suboscines (Baptista and Kroodsma dade Estadual de Londrina, Londrina—PR 86051-980, Brazil. 6 31 School Sreet, Hatfield, MA 01038, USA (deceased). 8 Conservation Science Program, World Wildlife Fund, 7 College of Natural Sciences and Mathematics, Califor- 1250 24th Street NW, Washington, D.C. 20037, USA. nia State University, Sacramento, CA 95819, USA. 9 Corresponding author; e-mail: [email protected] 1 The Wilson Journal of Ornithology wils-125-01-01.3d 19/12/12 19:29:28 1 Cust # 12-033 2 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 125, No. 1, March 2013 2001). Our fascination with this question no doubt from one bird to the next along a transect insuring lies in our own human elaboration of vocal that each new bird was different from the one learning through speech, and the absence of such before. Most of our analyses are based on males elaborated vocal learning in our close primate who sang the ‘‘Monteverde dialect’’ (below), and relatives (but see Crockford et al. 2004). Vocal the number of adult males with Monteverde songs learning also occurs among some other mammals, that were recorded throughout the years was: 1974 such as certain whales (Noad et al. 2000) and bats (5), 1981 (1), 1985 (7), 1986 (2), 1987 (1), 1988 (Boughman 1998, Knornschild et al. 2010). (9), 1989 (1), 1991 (2), 1998 (3), 1999 (4), 2000 Such evolutionary questions are difficult to (15), 2001 (19), 2002 (14), 2006 (3), 2011 (14). answer, not only because vocal learning arose so Of particular interest in these Monteverde songs far back in time that we cannot reconstruct the was the frequency of their intensely loud tonal conditions under which selection for this trait notes (hereafter ‘Whistles’); the number of occurred, but also because surveys for vocal Whistles measured for each male ranged from learning among extant animal groups are incom- 2-191 (mean 31.7). plete. Among birds, for example, lack of vocal A variety of recorders and microphones was learning among suboscines is often inferred for used, but when we needed precise temporal and the entire group from studies of only a few species frequency measurements, we used primarily (Raposo and Ho¨fling 2003). digital recordings made on an HHB Portadat Here we provide behavioral evidence for song PDR-1000 (1999–2002) and a Sound Devices learning among Procnias bellbirds, cotingas that 722 (2011). Parabolic microphones were essen- are firmly embedded within the suboscine Tyr- tial to record the exceptionally soft elements in anni. Among birds, this is a more recent origin of the songs, and from 1999–2002 we used a vocal learning than occurred among ancestral Telinga Pro5W parabolic microphone, and during songbirds, parrots, or hummingbirds, giving hope 2011 a Telinga Universal with a Sennheiser that a comparative survey among the suboscine MKH20. cotingas may help reveal the conditions under Other recordings used in this study came from a which vocal learning evolved. variety of sources. Those from the British Library included recordings archived by Barbara Snow METHODS in 1974; the Macaulay Library at the Cornell During July 1999–2002, and again in 2011, Laboratory of Ornithology provided a number, male Three-wattled Bellbirds (Procnias tricarun- including those by Trainer from the 1980s. For culata) were recorded intensively at Monteverde, these recordings, professional analog recorders Costa Rica. Each recorded bird was classified by were used, and the recorded birds were identified plumage into one of three groups: two or and described; slightly varying analog tape three years old (with yellowish-green streaked speeds could have introduced small errors into plumage); four, five, or six years old (with these recordings, and we are mindful of that as increasing amounts of white and chestnut plum- we interpret song differences over time. In age); or adult, with pure chestnut and white Nicaragua during July 2001, we used Sony plumage and long wattles. (The aging scheme is TCD5ProII analog recorders and Telinga Pro5W based on plumage changes in banded birds from microphones to record four males. At Monte- hatching to at least seven years, when males reach verde during April 2006, Kroodsma used a Sony adult plumage; D. Hamilton, unpubl. data.) We MZN-707 minidisc and Sennheiser ME66 to did not analyze recordings of unseen birds. record three adult males. During each year of intensive sampling, we As an index of how the songs of the took care to include each male only once in the Monteverde dialect changed from 1974 to 2011, analyses. A number of birds were banded and we measured the frequency of the songs’ loud could always be identified as individuals (at least Whistles with the ‘Max Frequency’ (frequency of eight in our recorded samples, out of 151 that had peak power) feature on Raven software (with been caught in canopy nets and banded at ‘‘spectrogram window size’’ of 66,536, yielding a Monteverde; for methods, see Powell and Bjork frequency resolution of ,1 Hz). Song compo- 2004). Others were identified by location and nents other than the loud whistles also changed favorite singing perches, often well-separated over the years, and we describe them where we from other singers. Other times we could walk can, but we found it difficult to characterize The Wilson Journal of Ornithology wils-125-01-01.3d 19/12/12 19:29:30 2 Cust # 12-033 Kroodsma et al. N SONG LEARNING IN SUBOSCINE BELLBIRDS 3 FIG. 1. The ‘Bonk-swish-Whistle-swish’ song of the Monteverde dialect of the Three-wattled Bellbird. The basic form of the song has stayed the same from 2002–2011: songs begin with a loud Bonk (B), contain a loud Whistle (W) mid-way, and have soft swishing elements before and after the Whistle. Songs from the two males within each year are essentially identical to each other, but notable changes occurred from 2002 to 2011: By 2011, the Whistle is about 450 Hz lower in frequency; elements a, b, and c have been extended to about three times the duration (designated by a ‘prime’ in 2011); and element b has been transformed in quality. Another song of the Monteverde dialect (‘Bonk-swish-swish’) omits the section marked by an arrow in the upper left sonagram. In typical sonagrams, the louder the song element the darker the image, but in these and other sonagrams the especially quiet elements (all those not designated with a capital letter) have had to be darkened so that they would show. satisfactorily and systematically changes in either RESULTS the loud, complex Bonks of the Monteverde Description of Adult Bellbird Songs dialect or the songs’ softer sounds that are so difficult to record. The ‘Monteverde Dialect.’—At Monteverde, In Arapongas, Brazil, Fandin˜o-Marin˜o walked Costa Rica, during July of the years 1999–2002 the streets of town during 1998, listening to and 2011, about three-quarters of adult males (73 sounds of captive Bare-throated Bellbirds (Proc- of 101 encountered, or 72%) sang only what has nias nudicollis) that many aviculturists kept in the come to be called the ‘Monteverde dialect.’ town.