Gaudy Juvenile Plumages of Cinereous Mourner (Laniocera hypopyrra) and Brazilian Laniisoma (Laniisoma elegans) Author(s): Fernando Mendonça D'Horta, Guy M. Kirwan, and Dante Buzzetti Source: The Wilson Journal of Ornithology, 124(3):429-435. 2012. Published By: The Wilson Ornithological Society DOI: http://dx.doi.org/10.1676/11-213.1 URL: http://www.bioone.org/doi/full/10.1676/11-213.1 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Published by the Wilson Ornithological Society VOL. 124, NO. 3 September 2012 PAGES 429–650 The Wilson Journal of Ornithology 124(3):429–435, 2012 GAUDY JUVENILE PLUMAGES OF CINEREOUS MOURNER (LANIOCERA HYPOPYRRA) AND BRAZILIAN LANIISOMA (LANIISOMA ELEGANS) FERNANDO MENDONÇA D’HORTA,1,4 GUY M. KIRWAN,2 AND DANTE BUZZETTI3 ABSTRACT.—We describe the juvenile plumages of the Cinereous Mourner (Laniocera hypopyrra) and the Brazilian Laniisoma (Laniisoma elegans). Both L. hypopyrra and L. elegans possess a dramatically conspicuous plumage as juveniles in contrast to the generally cryptic plumage pattern exhibited by most juvenile birds. They are predominantly covered by cinnamon-orange feathers with black terminal spots, contrasting with the nest and the predominant colors of their environment. This colorful plumage presumably makes them more at risk from predation by visually oriented animals (e.g., raptors and primates), during one of the most vulnerable phases of their life, and strongly suggests these plumages function as a true, or false (mimicry), signal of ‘unprofitability’. Previous knowledge concerning the phylogenetic relationships between these two genera, and the juvenile plumage patterns of other species placed in the Tityridae indicate this shared character in L. hypopyrra and L. elegans represents a synapomorphy within this clade, thereby providing additional evidence of their relationship. Received 13 December 2011. Accepted 1 May 2012. The neotropical genera Laniocera and Laniisoma are strictly forest birds (Stotz et al. 1996). The genus Laniocera comprises two species, Cinereous Mourner (L. hypopyrra), which is widely distributed over the greater part of Amazonia with a geographically separate population in the central Atlantic Forest, and the Speckled Mourner (L. rufescens), which occurs over Middle America and northwest South America (Ridgely and Tudor 1994, Fitzpatrick et al. 2004). Laniisoma is usually 1 Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, 05508-090, São Paulo, SP, Brazil. 2 Research Associate, Field Museum of Natural History, 1400 South Lakeshore Drive, Chicago, IL 60605, USA. 3 Rua Álvaro Rodrigues 163, sala 4, 04582-000, São Paulo, SP, Brazil. 4 Corresponding author; e-mail: fmhorta@usp.br considered to be a monospecific genus (e.g., Snow 1982, 2004), although some authorities have separated its Andean and Atlantic Forest populations at the specific level. We treat Laniisoma elegans as a polytypic species following Kirwan and Green (2011, contra the IOC: Gill and Donsker 2012) that is discontinuously distributed in the Brazilian Atlantic Forest as well as even more disjunctly in the foothills of the Andes, from southwest Venezuela south to northern Bolivia (Ridgely and Tudor 1994, Snow 2004). The taxonomic affinities of Laniocera and Laniisoma have been the subject of controversy and speculation (e.g., Traylor 1979, Prum and Lanyon 1989, Sibley and Ahlquist 1990, Fitzpatrick et al. 2004, Snow 2004). Prum and Lanyon (1989), in a phylogenetic study of what they termed the ‘Schiffornis group’, used morphological characters and were the first to identify a 429 430 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 124, No. 3, September 2012 monophyletic group formed by Schiffornis, Laniocera, and Laniisoma. The evolutionary relationships among these three genera were subsequently confirmed by Barber and Rice (2007) based on a molecular phylogeny of the Tityridae, as well as by the more inclusive phylogenetic study of Tello et al. (2009). The clade comprising Schiffornis, Laniisoma, and Laniocera was strongly supported by both studies, and was grouped by Barber and Rice (2007) under the subfamily Laniisominae. These studies suggested that Lanisoma and Laniocera were sisters with Schiffornis being sister to these two genera. Other characters also support recognition of the subfamily Laniisominae. There are some similarities between known nests among Laniisominae species, but these have not been described for all species (or even genera), preventing a more complete understanding of the evolution of these characters. However, available information suggests nests of Laniocera spp. (only that of L. hypopyrra is known) and Schiffornis spp. are quite similar. Only the nest of Thrush-like Schiffornis (Schiffornis turdina) has been described in detail to date, but some data are available for Greenish Schiffornis (S. virescens). All nests described have been characterized basically as large, bulky cups of dry leaves (Skutch 1969, Londoño and Cadena 2003, Snow 2004). However, the nest of Laniisoma remains undescribed. The eggs of S. turdina are similar to those of L. hypopyrra in coloration, but this similarity cannot be interpreted as an indication of evolutionary affinity because this character is highly homoplasic (Londoño and Cadena 2003). The juvenile plumages of many neotropical bird species are relatively well known. The juvenile plumages among species of Tityridae, as in the great majority of birds, are inconspicuous. The juvenile, even in Schiffornis, described for S. turdina, resembles the adult (Wetmore 1972, Kirwan and Green 2011). Contrasting with this general pattern we describe the colorful juvenile plumages of Laniocera hypopyrra and Laniisoma elegans, compare them with other species of Tityridae, and discuss their evolutionary and ecological significance. METHODS The description of the juvenile plumage of Laniocera hypopyrra is based on a specimen collected on 6 September 2002 by FMH in the understory of a disturbed terra firme forest, at Igarapé Mutum, Juruti, Pará, east Amazonian Brazil (02u 369 S, 56u 139 W). The specimen (Frontispiece, Fig. 1) is housed at the Museu Paraense Emı́lio Goeldi Belém, Brazil (MPEG 56.746). We describe the previously unknown juvenile plumage of Laniisoma e. elegans, based on an observation by Jeremy C. Minns (in litt. to GMK, May 2008) in the Atlantic Forest at the Parque Estadual da Serra do Mar, Núcleo Santa Virgı́nia, São Luiz do Paraitinga, São Paulo (23u 239 S, 45u 089 W), southeast Brazil, on 30 December 1997. We also recapitulate a description of the nestling (pullus) of L. e. buckleyi, based on the two syntypes (Figs. 2, 3) of this taxon at The Natural History Museum, Tring, UK (BMNH 1888.1.20.337 and BMNH 1888.1.20.338), both of which were collected by Clarence Buckley at Pindo, Ecuador, and described by P. L. Sclater to illustrate plumage progression in Laniisoma. Pindo is an untraced locality, speculated by Paynter (1992) to be the Rı́o Pindo (03u 509 S, 79u 459 W) in Pastaza. This remarkable plumage also was illustrated in Sclater and Salvin (1880: plate 16) and Snow (1982:34, plate 2). RESULTS Laniocera hypopyrra.—The L. hypopyrra specimen (MPEG 56.746) possesses typical adult flight feathers; the remiges and rectrices being primarily gray, while the median and greater wing-coverts, tertials, and rectrices are adorned with pale cinnamon spots on their tips. The entire body, except for the flight feathers, is covered by bright orange feathers with black terminal spots (Fig. 1), while the head is covered by a crest, also formed of orange feathers with black terminal spots. A remarkable feature of the crest is the feathers in which there are distal extensions, composed by up to six orange filaments 15 to 22 mm long, possessing white distal and proximal portions (Frontispiece, Fig. 1). The crest, including these filaments, reaches 40 to 48 mm. The same structure is exhibited by some of the dorsal feathers. Subadults (and juveniles) of L. hypopyrra exhibit a few, irregular, bright orange feathers with black terminal spots in a seemingly random fashion across their underparts, as well as parts of the upperparts, especially when younger (Kirwan and Green 2011). Laniisoma elegans.—The two syntypes of L. e. buckleyi are basically identical to each other. They are very similar to L. hypopyrra in some d’Horta et al. N JUVENILE PLUMAGES OF LANIOCERA AND LANIISOMA 431 FIG. 1. Ventral (A) and dorsal (B) view of juvenile specimen of Laniocera hypopyrra. plumage features, mainly in the upperparts. The plumage of the dorsal region is mostly cinnamon, as well as the head and throat with black subterminal bars and small white tips to the feathers. The rest of the underparts are primarily dark gray to blackish barred off-white, especially broadly over the breast with cinnamon-orange fluffy feathers on the flanks, and especially in the ventral region. The wing-coverts are very dark olive-green, marked with a few irregular rufous spots, while the tertials and flight feathers (which were no longer in pin) are broadly fringed brighter olive-green. Filamentous down feathers similar to those observed in L. hypopyrra sprout to 20– 26 mm from the head and body, form noticeable tufts in places, and are either black with white tips, on the head, or cinnamon with white tips, over the back (Figs. 2, 3). J. C. Minns observed an adult (perhaps subadult) female L. e. elegans, which was subsequently joined by a fledged juvenile of the same species. He described the latter bird as being the same size as the adult or subadult, but the entire body was mottled dark green-brown, which color seemed almost black in some light, and rufous. The mottling took the form of large asymmetric patches, while Minns noted the feathers on the head and around the base of the bill were erect and spiky. DISCUSSION Evolution of Juvenile Plumage.—Adults of Laniocera and Laniisoma exhibit significant 432 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 124, No. 3, September 2012 FIG. 2. Dorsal (A) and ventral (B) view of nestling specimens of Laniisoma elegans (Guy M. Kirwan/E The Natural History Museum, Tring, United Kingdom). differences in some morphological traits (e.g., plumage), which resulted in earlier misinterpretations concerning their taxonomic affinities (Snow 2004). However, Prum and Lanyon (1989), based on a morphological phylogeny, suggested Laniocera and Laniisoma are sister taxa with the genus Schiffornis sister to the Laniocera-Laniisoma clade. This hypothesis was corroborated by two molecular phylogenies (Barber and Rice 2007, Tello et al. 2009). A similarly bulky nest occurs in several species although nesting is incompletely known for all taxa (Londoño and Cadena 2003). The juvenile/immature plumage usually resembles that of the adult female in all of the other species currently placed in the Tityridae, i.e., Tityra spp., purpletufts (Iodopleura spp.), becards (Pachyramphus spp.), White-naped Xenopsaris (Xenopsaris albinucha), Myiobius spp., Terenotriccus spp., royal-flycatchers (Onychorhynchus spp.), Sharpbill (Oxyruncus cristatus), and the Schiffornis spp. Not all of these taxa are universally accepted to be part of the Tityridae with, for instance Oxyruncus cristatus, at times being accorded its own family, Oxyruncidae (e.g., Kirwan and Green 2011, Remsen et al. 2011). Many of these species present juvenile/immature plumages that are even more inconspicuous than those of females, exhibiting darker (Tityra spp.), browner (Xenopsaris albinucha), or more greenish (Barred Becard, Pachyramphus versicolor) plumage. The differences between juveniles and females in other species, are chiefly reflected in the most colorful tracts of plumage, for instance Blacktailed Myiobius (Myiobius atricaudus), in which the juvenile lacks yellow in the coronal patch, or in Oxyruncus cristatus, in which juveniles lack any red or orange in the crown. The only group that presents conspicuous marks in their plumage is the genus Iodopleura. Juveniles of two of the three species—White-browed Purpletuft (I. isabellae), and Buff-throated Purpletuft (I. pipra)— possess rather conspicuous, white- or buff-tipped feathers, but do not resemble the juveniles of L. hypopyrra and L. elegans. The juvenile of the Dusky Purpletuft (I. fusca) is presently unknown, although the nest has been recently described, and is identical to those of the other two species (Ingels and Vinot 2010). We suspect the juvenile of this species is unlikely to differ greatly from the d’Horta et al. N JUVENILE PLUMAGES OF LANIOCERA AND LANIISOMA 433 FIG. 3. Image of pullus and adult Laniisoma elegans, originally published in the Proceedings of the Zoological Society of London for 1880 (plate 18). Courtesy of Biodiversity Heritage Library, Zoological Society of London. http://www. biodiversitylibrary.org/ 434 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 124, No. 3, September 2012 pattern exhibited by the other two species of Iodopleura. Juveniles, as far as is known, resemble females even in Schiffornis, the most closely related genus to Laniocera and Laniisoma, although Kirwan and Green (2011) speculate that Varzea Schiffornis (S. major) with drop-shaped bluish-gray spots on the greater wing-coverts perhaps represents the juvenile plumage. Thus, the general pattern of juvenile plumage observed in Tityridae, as for most birds, is less conspicuous, contrasting dramatically with those plumages we describe for L. hypopyrra and L. elegans. The evolutionary relationship between L. hypopyrra and L. elegans, when considered with respect to juvenile plumages of other Tityridae, strongly suggests the described state is a synapomorphy of the clade Laniocera-Laniisoma. Thus, we expect the first plumage (juvenile) of Laniocera rufescens should possess a similar plumage pattern. This species’ nest has not been found (Fitzpatrick et al. 2004, Kirwan and Green 2011), but there are descriptions of so-called juvenile plumage in the literature. Some authors have suggested the juvenile is grayer on the head with black fringes to the greater and median wing-coverts, and randomly black-spotted body-sides (Restall et al. 2006), while the immature is reported to resemble the female, albeit with more prominent wing and underparts markings, a grayish wash to the crown, foreneck, lower back and rump and, at times with some sparse black spotting on the breast with dull gray bands extending from the neck-sides to the undertail coverts (Wetmore 1972, Hilty and Brown 1986, Fitzpatrick et al. 2004). We suspect that all of the descriptions concerning non-adult plumages of L. rufescens refer to plumage states older than juvenile given the documented juvenile plumages of L. hypopyrra and Laniisoma elegans described in this paper. Ecological Function.—Coloration among bird species is often subject to differences, occasionally extreme, dependent on sex, season, and age. The general pattern related to plumage of immatures, regardless of sex, is characteristically dull, or inconspicuously marked, and closely resembling the plumage of the adult female (Kilner 2006). Predators can threaten birds of all ages, but they pose the greatest threat to eggs, nestlings, and young juveniles (Dumbacher and Pruett-Jones 1996), which are more vulnerable than adults. The evolution of the inconspicuousness of juvenile plumage is considered to be a consequence of selection for crypsis (Kilner 2006) in response to predation pressure by visually oriented predatory species (e.g., raptors and primates). The juveniles of Laniocera hypopyrra and Laniisoma elegans, in contrast to the general pattern of plumage color observed in juvenile birds, possess highly conspicuous plumages, while adults of both species are either very inconspicuous or less conspicuous, respectively. Snow (1982) suggested the nestling of Laniisoma elegans had evolved to appear like moss covered by fruits, and subsequently postulated this remarkable plumage represents an adaptation to the species using an exposed nest site (Snow 2004). However, we consider the patterns observed in the juveniles of these two species (and the nestling of Laniisoma) strongly suggest either a chemical defense (toxic and/or unpalatable) or Batesian mimicry (e.g., of a large, hairy caterpillar). A general pattern of conspicuous colors, exhibited by some birds, may function as a signal of ‘unprofitability’ to predators (Baker and Parker 1979). Chemical defense (toxic and unpalatable) in some taxa is correlated with aposematic coloration (Cott 1940, Cott and Benson 1970, Guilford 1990, Dumbacher and Pruett-Jones 1996). Some non-toxic or palatable species also present morphological and behavioral characters similar to those of toxic or unpalatable species by Batesian mimicry (Diamond 1982, Bortoloti 2006). Additionally, it has often been suggested that warning colors can also have a disruptive (Tullberg et al. 2005), or a distractive function (Stevens and Merilaita 2009). Further work is needed to test the alternative hypothesis regarding the ecological role of juvenile plumage of Laniocera and Laniisoma. ACKNOWLEDGMENTS Personnel from CNEC Engenharia Ltd. supported FMH’s fieldwork. We are grateful to Manuel Santa Brı́gida who prepared the specimens collected during the same fieldwork, and Alexandre Aleixo from MPEG, who provided the specimen loan. Jeremy C. Minns is warmly thanked for sharing his observations of the juvenile of Laniisoma elegans. GMK is grateful to Robert Prŷs-Jones, Mark Adams, and Hein van Grouw at The Natural History Museum, Tring, for permission to study relevant specimen material housed there. 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