Species delimitation in the White-faced Cuckoo-dove (Turacoena manadensis) based on bioacoustic data
© Ng and Rheindt. 2016
Received: 4 August 2015
Accepted: 21 December 2015
Published: 26 January 2016
The White-faced Cuckoo-dove (Turacoena manadensis) is a poorly-known Wallacean endemic with a limited distribution on Sulawesi and its satellites, including the Togian, Banggai and Sula archipelagoes. In 1900, populations from the Sula archipelago were awarded subspecies status T. manadensis sulaensis based on smaller size and minor differences in plumage; however, this distinction has not been corroborated subsequently, and T. manadensis is considered by most modern sources to be monotypic across its range.
We conducted vocal analysis of the cuckoo-doves’ main song using recordings collected from across the taxon’s natural range. Descriptive information on the songs was obtained from the recordings using bioacoustic analysis software, after which several statistical methods were used to investigate differences in vocalizations among populations.
We report deep bioacoustic divergences in vocal trait pattern from across the cuckoo-doves’ range, with birds from Peleng and Taliabu in the east having a different vocal trait pattern from birds from Sulawesi, Buton, and Togian in the west. These patterns agree with changes in landmass that accompanied the sea level fluctuations caused by Pleistocene glacial cycles, and indicate that eastern and western cuckoo-dove populations are at the level of different biological species.
We propose that the eastern taxon be elevated to species level as T. sulaensis. Given the rampant degree of habitat destruction in its limited range, this taxonomic change will have important implications on the conservation status of T. sulaensis.
KeywordsWallacea Sulawesi Peleng Taliabu Buton Pleistocene Island biogeography
Wallacea, bound by Wallace’s Line in the West and Lydekker’s Line in the East, is widely recognized as one of the world’s leading biodiversity hotspots (Mittermeier et al. 1999; Myers et al. 2000). The area has very high levels of vertebrate endemism, with about 40 % of known bird species, more than 60 % of the known mammal, amphibian, and reptile species, and 75 % of known fish species found nowhere else (Sodhi et al. 2004; Lohman et al. 2011). One of the primary mechanisms leading to the rich biodiversity of the region is its complex earth history. On the one hand, Wallacea is characterized by unusually rapid tectonic movements, making it one of the only areas on earth where the distribution of land masses has changed dramatically within the last ~5 mya (Hall 1998, 2002, 2012). On the other hand, Wallacea has endured the repeated appearance and disappearance of land bridges between some of its landmasses during the sequential ~120 m sea level changes in the last 2.5 mya (Voris 2000; Siddall et al. 2003; Caputo 2007), subjecting populations to alternating cycles of isolation and contact, and turning Wallacea into a natural laboratory for evolution and speciation. Despite this, there has been a paucity of biodiversity research conducted in the region and Wallacean biodiversity is in general poorly understood (Lohman et al. 2011).
The White-faced Cuckoo-dove (Turacoena manadensis) (Quoy and Gaimard 1830) is a Wallacean endemic inhabiting Sulawesi and its satellites, including the Togian, Banggai and Sula archipelagoes. These birds are arboreal frugivores (Baptista et al. 2013) and can be found in a wide range of habitats from primary forests to degraded orchards, where they help as seed dispersers of a range of tree and plant species. They have been documented ranging up to 500 m above sea level on Taliabu and to over 900 m on Peleng (Rheindt 2010; Rheindt et al. 2010).
The species was first described as Columba manadensis (Quoy and Gaimard 1830) based on a specimen from Manado, now stored at the Muséum National d’Histoire Naturelle in Paris (Voisin et al. 2005). Bonaparte then divided it off into the genus Turacoena in 1854 (Bonaparte 1854). Forbes and Robinson (1900) allocated populations from the Sula archipelago subspecies status T. manadensis sulaensis based on smaller size and minor differences in plumage (Forbes and Robinson 1900). However, this distinction has not been corroborated subsequently, and T. manadensis is considered by most modern sources to be monotypic (White and Bruce 1986; Coates and Bishop 1997; de By 2002; Gibbs 2010; Clements et al. 2012; Baptista et al. 2013).
We analyzed a dataset of sound recordings of the White-faced Cuckoo-dove collected by us (e.g. Rheindt 2010; Rheindt et al. 2010, 2014) and other field ornithologists, and spanning several island groups including the ranges of both the often-synonymized subspecies sulaensis as well as the nominate. Vocal analyses can be more diagnostic compared to morphology as species delimitation tools in pigeons and doves: many columbid species differ only in minute plumage details from one another but have completely different, innately-coded vocalizations, e.g. the Streptopelia radiation in Africa (de Kort and ten Cate 2001; Johnson et al. 2001; Sinclair et al. 2003), several Patagioenas species in South America (Mata et al. 2006), and several Ptilinopus members in South-east Asia (Rheindt et al. 2011). This makes vocal traits even more important in columbid taxonomy than in oscines. We report on distinct variation in the vocalizations of the White-faced Cuckoo-dove from across its geographic range in Wallacea, which provides new insights into species boundaries within this complex. The objectives of our publication are to (1) document the vocal character differences, (2) combine the differences in vocal trait pattern with Pleistocene earth-historic information to revise species limits in this taxon, and (3) explore the implications this would have on the conservation status of the taxa nestled within the complex.
Bioacoustic sample collection
RavenLite 1.0 (Cornell Lab of Ornithology, Ithaca, NY, USA) was used to collect descriptive information from the bird calls. A set of 16 vocal characters covering both temporal and frequency-based parameters was measured: (1) number of elements within SM1, (2) number of elements within SM2, (3) duration of SM1, (4) duration of SM2, (5) average element duration across SM1, (6) average element duration across SM2, (7) lowest frequency across SM1, (8) lowest frequency across SM2, (9) highest frequency across SM1, (10) highest frequency across SM2, (11) frequency range of SM 1, (12) frequency range of SM2, (13) dominant frequency of SM1, (14) dominant frequency of SM2, (15) first element duration of SM2, and (16) the inter-motif break duration.
For all recordings containing multiple call bouts, at least three measures for the same character were taken for each individual. In situations where there were large variations in parameter measurements, additional calls (up to 8) were analysed to maximize accuracy.
We generated boxplots for each of the vocal characters using R (R development core team 2008). We performed principal component analysis (PCA) on the resultant 16-character data matrix using the software XLSTAT (Addinsoft 2012). In order to prevent skewing of the results, only individuals with full call data (sample size n = 24) were used for the PCA.
A master sheet of the measurements that were taken during the primary data collection can be found in the Additional file 1: Appendix.
Due to SM1 having a shorter duration and lesser amplitude than SM2, the signal from SM1 was lost in approximately 30 % of the lesser-quality recordings. Overall, full call data (i.e. SM1 and SM2) were obtained for 24 out of the 34 individuals, comprising 70 % of the full dataset. For the remaining 10 individuals, only SM2 call data were obtained.
In contrast, the calls of satellite birds comprise more elements in both SM1 and SM2. SM1 of satellite birds comprises 3.78 ± 1.35 elements, while SM2 comprises 6.02 ± 1.83 elements. These differences in the number of elements translate directly into much longer call durations for SM1, SM2 and the full call (SM1 duration of 0.52 ± 0.16 s, SM2 duration of 1.97 ± 0.36 s, full call duration of 2.57 ± 0.39 s; see Additional file 1: Appendix).
Inter-taxon comparisons of all 16 parameters using Isler’s criterion analysis for diagnosability
Parameters (total n = 24)
Peleng (n = 9)
Taliabu (n = 4)
Sulawesi (n = 8)
SM1 number of elements
SM2 number of elements
Total call duration
Peleng (n = 9)
Taliabu (n = 4)
Sulawesi (n = 8)
Togian (n = 3)
SM1 low frequency
SM1 high frequency
SM1 frequency range
SM1 dominant frequency
SM1 average element duration
Inter-motif break duration
SM2 low frequency
SM2 high frequency
SM2 frequency range
SM2 dominant frequency
SM2 1st element duration
Peleng (n = 9)
Taliabu (n = 4)
Sulawesi (n = 8)
Togian (n = 3)
We provide documentation of the call of the White-faced Cuckoo-dove from different localities across its natural range in Wallacea: Togian island, Buton island, Sulawesi, Peleng in the Banggai archipelago, and Taliabu in the Sula archipelago (Fig. 1). Two vocal types exist, with deep bioacoustic differentiation separating the nominate populations of Sulawesi/Buton and Togian from satellite populations inhabiting the Banggai and Sula archipelagoes to the east.
The five vocal characters which showed diagnosability are all temporal in nature: the number of elements in SM1, total duration of SM1, number of elements in SM2, total duration of SM2, and total call duration (Fig. 4; Table 1). The remaining three temporal parameters (inter-motif duration, SM1 and SM2 average element lengths) were not informative. None of the eight frequency measures were sufficiently differentiated to be informative (data not shown). This is in agreement with earlier observations of frequency parameters being less informative than temporal parameters in several columbid genera including Turacoena, Ptilinopus, and Streptopelia (Beichle 1989; Slabbekoorn and Ten Cate 1999; Rheindt et al. 2011).
Vocal patterns agree with Pleistocene sea level changes
Species status of the White-faced Cuckoo-dove
Vocal differentiation in doves and other birds often is accompanied by genetic distinctiveness as these birds have innate songs that cannot be learned during their lifetimes (Lade and Thorpe 1964; Nottebohm and Nottebohm 1971; de Kort et al. 2002; Marler and Slabbekoorn 2004). Additionally, vocal differentiation is particularly indicative of species limits within the pigeons and doves: there are many examples of unequivocally recognized, distinct species sharing little differences in plumage but exhibiting drastically different vocalizations, resulting in vocal data being routinely used in taxonomic decisions pertaining to this family (Columbidae) (Sinclair et al. 2003; Mata et al. 2006; Rheindt et al. 2011). Our findings suggest that the nominate and satellite populations of White-faced Cuckoo-dove are highly differentiated, and modern taxonomic treatment of T. manadensis as a single species across its range is inaccurate. Instead, the satellite group should be considered a separate allopatric species from the nominate T. manadensis under both the Biological Species Concept (Mayr 1963, 1996) and the Phylogenetic Species Concept (Cracraft 1983). As the satellite taxon was formerly classified as subspecies sulaensis, we propose that this taxon be upgraded to full species status. Forbes and Robinson (1900) restricted the name sulaensis to the Sula Islands, but our bioacoustic results leave no doubt that the name must also be applied to populations on the Banggai archipelago. In the future, additional genetic, morphological, and behavioural data on these taxa should be gathered, analyzed, and compared in an integrative taxonomical framework, and these two cryptic sister species further characterized.
The re-drawing of biological species limits in the white-face cuckoo-dove complex has implications on the conservation status of the taxa nestled within it. The International Union for the Conservation of Nature (IUCN) allocates conservation status to species depending on several criteria including population and distribution sizes and trends. When Turacoena manadensis was last assessed in May 2012, it was given the status “Least Concern” based on several population and range distribution criteria: a stable population size exceeding 10,000 individuals, a stable geographical range exceeding 20,000 km2, and habitat that was not deemed to be excessively fragmented (BirdLife International 2012; IUCN 2012). With Turacoena sulaensis found to be sufficiently diverged to form a separate species, however, the “Least Concern” status may no longer apply to this taxon. The Banggai and Sula archipelagoes have a total land area of about 13,000 km2 (Google Earth 2014), which marks the maximum extent of this taxon, and is substantially smaller than the 20,000 km2 range requirement for a species be listed as “Least Concern”. Additionally, habitat quality on these islands has deteriorated drastically in the past few decades as a result of logging, agricultural practices, and forest fires (Rheindt 2010; Rheindt et al. 2010). While the White-faced Cuckoo-dove has been observed utilising secondary forest and abandoned orchards (Baptista et al. 2013), the latter habitats probably represent sink rather than source habitats and are unlikely to harbour the stronghold of this species. On Peleng, the lowlands are largely devoid of forests, with substantial secondary growth found only above 600 m and primary growth found only above 800 m above sea level where the species is much rarer than below (Rheindt et al. 2010). The situation on Taliabu is even more dire: lowland forest is virtually gone, high-altitude forests (above 750 m above sea level) are highly degraded, and untouched montane forest patches, even small ones, are perilously rare (Rheindt 2010). T. sulaensis thus fulfils IUCN’s criterion B1(b) for a conservation status of “Vulnerable”, as there is continuing decline of its extent of occurrence as well as its area and quality of habitat. Future studies need to be carried out to ascertain if the species experiences extreme fluctuations in extent of occurrence, area of occupancy, number of locations or subpopulations, or number of mature individuals, which constitute criterion B1(c); such studies will be able to determine if the taxon indeed qualifies as “Vulnerable”. In the interim, we propose that T. sulaensis be classified as “Near Threatened”.
Using highly diagnostic vocalization data, we have demonstrated that two distinct species of White-faced Cuckoo-dove exist across its natural range in Wallacea: nominate taxon T. manadensis from Sulawesi and the Togian archipelago, and satellite taxon T. sulaensis from the Banggai and Sula archipelagoes to the east. These patterns of divergence agree with the presence and absence of land bridges between islands in the region resulting from sea level changes during Pleistocene glaciations. These changes to the taxonomic status of the White-faced Cuckoo-dove have important implications on the conservation statuses of the taxa nestled within.
FER conceived and designed the research, and collected field recordings. NSRN performed the analyses, after which FER and NSRN interpreted the results. The manuscript was written by NSRN. Both authors read and approved the final manuscript.
We thank all the recordists for their generous contributions, especially James A. Eaton and Rob O. Hutchinson, and the many other individuals who contributed their recordings to online sound libraries. We also thank Emilie Cros and Keren Sadanandan of the Avian Evolution Lab, NUS for their patient help and advice with the manuscript.
The authors declare that they have no competing interests.
Work for this project was funded by National University of Singapore internal Faculty of Sciences Grant WBS R-154-000-570-133 and Department of Biological Sciences grant WBS R-154-000-583-651.
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- Addinsoft SARL. XLstat 2012: Leading data analysis and statistical solution for microsoft excel. Addinsoft SRL. 2012.Google Scholar
- Baptista LF, Trail PW, Horblit HM, Kirwan GM. White-faced Cuckoo-dove (Turacoena manadensis). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E, editors. Handbook of the birds of the world Alive. Barcelona: Lynx Edicions; 2013.Google Scholar
- Becker JJ, Sandwell DT, Smith WHF, Braud J, Binder B, Depner J, Fabre D, Factor J, Ingalls S, Kim SH, Ladner R, Marks K, Nelson S, Pharaoh A, Trimmer R, Von Rosenberg J, Wallace G, Weatherall P. Global bathymetry and elevation data at 30 arc seconds resolution: SRTM30_PLUS. Mar Geod. 2009;32(4):355–71.View ArticleGoogle Scholar
- Beichle U. Acoustical features of the six species of pigeons of the Samoan Islands. J Ornithol. 1989;130:3435–51.View ArticleGoogle Scholar
- BirdLife International. Turacoena manadensis. The IUCN Red list of threatened species version 20143. http://www.iucnredlist.org (2012). Accessed 1 Apr 2015.
- Bonaparte CLJL. Compte Rendus Hebdomadaire des Séances de l’Académie des Sciences 39: 1112. Paris: Institut De France (Paris) Académie des Sciences; 1854.Google Scholar
- Caputo R. Sea-level curves: perplexities of an end-user in morphotectonic applications. Global Planet Change. 2007;57(3):417–23.View ArticleGoogle Scholar
- Clements JF, Schulenberg TS, Iliff MJ, Sullivan BL, Wood CL, Roberson D. The eBird/clements checklist of birds of the world: version 67. http://www.ebird.org (2012). Accessed 1 Apr 2015.
- Coates BJ, Bishop D. A guide to the Birds of Wallacea. Alderly: Dove Publishing; 1997.Google Scholar
- Cracraft J. Species concepts and speciation analysis. Current Ornithology. New York: Springer; 1983. p. 159–87.View ArticleGoogle Scholar
- de By RA. The Sibley/Monroe World List of Bird names. http://www.ornitaxacom/SM/SMOrg/sibley3html (2002). Accessed 1 Apr 2015.
- de Kort SR, ten Cate C. Response to interspecific vocalizations is affected by degree of phylogenetic relatedness in Streptopelia doves. Anim Behav. 2001;61(1):239–47.View ArticlePubMedGoogle Scholar
- de Kort SR, Den Hartog PM, Ten Cate C. Diverge or merge? The effect of sympatric occurrence on the territorial vocalizations of the vinaceous dove Streptopelia vinacea and the ring-necked dove S. capicola. J Avian Biol. 2002;33(2):150–8.View ArticleGoogle Scholar
- Forbes HO, Robinson HC. Catalogue of the Charadriomorphic birds (Charadriformes): auks (Alcidae), gulls (Laridae), and skuas (Stercorariidae)—Lari: lark-plovers (Thinocoridae), stone-curlews (Edicnemidae), jacanas (Jacanidae), sheathbills (Chionidae), crab-plovers (Dromadidae), coursers (Cursoriidae), plovers and snipes (Charadiidae)- Limicolae; pigeons (Columbae), and sand-grouse (Pterocles). Derby Museum Bull Liverp Museum. 1900;3:116–51.Google Scholar
- Gibbs D. Pigeons and Doves: a Guide to the Pigeons and Doves of the World. London: Bloomsbury Publishing; 2010.Google Scholar
- Google Earth. Version 7111888. http://www.googlecom/earth/indexhtml (2014). Accessed 29 Dec 2015.
- Hall R. Biogeography and Geological Evolution of SE Asia. Leiden: Backhuys Publishers; 1998.Google Scholar
- Hall R. Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions and animations. J Asian Earth Sci. 2002;20(4):353–434.View ArticleGoogle Scholar
- Hall R. Late Jurassic-Cenozoic reconstructions of the Indonesian region and the Indian Ocean. Tectonophysics. 2012;570–571:1–41.View ArticleGoogle Scholar
- Isler ML, Isler PR, Whitney BM. Use of vocalizations to establish species limits in antbirds (Passeriformes: Thamnophilidae). Auk. 1998;577–590.Google Scholar
- IUCN. IUCN Red List Categories and Criteria: Version 31. 2nd ed. Gland and Cambridge: IUCN; 2012.Google Scholar
- Johnson KP, de Kort S, Dinwoodey K, Mateman AC, ten Cate C, Lessells CM, Clayton DH. A molecular phylogeny of the dove genera Streptopelia and Columba. Auk. 2001;118(4):874–87.View ArticleGoogle Scholar
- Lade BI, Thorpe WH. Dove songs as innately coded patterns of specific behaviour. Nature. 1964;202:366–8.View ArticleGoogle Scholar
- Lohman DJ, de Bruyn M, Page T, von Rintelen K, Hall R, Ng PK, Shih H, Carvalho GR, von Rintelen T. Biogeography of the Indo-Australian archipelago. Annu Rev Ecol Evo S. 2011;42:205–26.View ArticleGoogle Scholar
- Marler PR, Slabbekoorn H. Nature’s Music: the Science of Birdsong. Waltham: Academic Press; 2004.Google Scholar
- Mata JR, Erize F, Rumboll M. Birds of South America: non-passerines: Rheas to Woodpeckers. New Jersey: Princeton University Press; 2006.Google Scholar
- Mayr E. Animal Species and Evolution. Cambridge: Belknap Press of Harvard University Press; 1963.View ArticleGoogle Scholar
- Mayr E. What is a species, and what is not? Philos Sci. 1996;63:262–77.View ArticleGoogle Scholar
- Mittermeier RA, Myers N, Mittermeier CG, Gil PR. Hotspots: earth’s biologically richest and most endangered terrestrial ecoregions. San Pedro Garza García: CEMEX; 1999.Google Scholar
- Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403(6772):853–8.View ArticlePubMedGoogle Scholar
- Nottebohm F, Nottebohm ME. Vocalizations and breeding behaviour of surgically deafened ring doves (Streptopelia risoria). Anim Behav. 1971;19(2):313–27.View ArticlePubMedGoogle Scholar
- Quoy JRC, Gaimard JP. Voyage de la corvette l’Astrolabe executé par ordre du roi, pendant 1826-1827-1828-1829. Atlas Ois. 1830;30:248.Google Scholar
- R Development Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org (2008). Accessed 20 Feb 2015.
- Rheindt FE. New biogeographic records for the avifauna of Taliabu (Sula Islands, Indonesia), with preliminary documentation of two previously undiscovered taxa. Bull Br Orn Club. 2010;130:33–51.Google Scholar
- Rheindt FE, Verbelen F, Putra DD, Rahman A, Indrawan M. New biogeographic records in the avifauna of Peleng Island (Sulawesi, Indonesia), with taxonomic notes on some endemic taxa. Bull Br Orn Club. 2010;130:181–207.Google Scholar
- Rheindt FE, Eaton JA, Verbelen F. Vocal trait evolution in a geographic leapfrog pattern: speciation in the Maroon-chinned Fruit Dove (Ptilinopus subgularis) complex from Wallacea. Wilson J Ornithol. 2011;123(3):429–40.View ArticleGoogle Scholar
- Rheindt FE, Prawiradilaga DM, Suparno Ashari H, Wilton P. New and significant island records, range extensions and elevational extensions of birds in eastern Sulawesi, its nearby satellites, and Ternate. Treubia. 2014;41:61–90.Google Scholar
- Siddall M, Rohling EJ, Almogi-Labin A, Hemleben C, Meischner D, Schmelzer I, Smeed DA. Sea-level fluctuations during the last glacial cycle. Nature. 2003;423(6942):853–8.View ArticlePubMedGoogle Scholar
- Sinclair I, Ryan P, Christy P, Hockey P. Birds of Africa: South of the Sahara. New Jersey: Princeton University Press; 2003.Google Scholar
- Slabbekoorn H, Ten Cate C. Collared dove responses to playback: slaves to the rhythm. Ethology. 1999;105(5):377–91.View ArticleGoogle Scholar
- Sodhi NS, Koh LP, Brook BW, Ng PK. Southeast Asian biodiversity: an impending disaster. Trends Ecol Evol. 2004;19(12):654–60.View ArticlePubMedGoogle Scholar
- Voisin C, Voisin JF, Jouanin C, Bour R. Liste des types d’oiseaux des collections du Museum National d’Histoire Naturelle de Paris, 14, Pigeons, Columbidae, deuxieme partie. Zoosystema. 2005;27(4):839–66.Google Scholar
- Voris HK. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr. 2000;27(5):1153–67.View ArticleGoogle Scholar
- Wallace AR. The Malay Archipelago. Oxford: John Beaufoy Publishing; 1869.Google Scholar
- White CMN, Bruce MD. The Birds of Wallacea (Sulawesi, the Moluccas & Lesser Sunda Islands, Indonesia): an annotated check-list. London: British Ornithologists’ Union; 1986.Google Scholar