ORNITOLOGIA NEOTROPICAL 15 (Suppl.): 73–81, 2004 © The Neotropical Ornithological Society

RECENT ANATOMICAL STUDIES ON NEOTROPICAL

Elizabeth Höfling

Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, n. 101, CEP 05508-900, São Paulo, Brazil. E-mails: [email protected] & [email protected]

Resumo. – Estudos anatômicos recentes de aves Neotropicais. – O conhecimento anatômico é um pré- requisito fundamental para entender as séries de transformações nos caracteres e a história evolutiva dos organismos. Os métodos tradicionais, utilizados no estudo anatômico, foram sendo gradualmente substi- tuídos por uma abordagem dinâmica e funcional, em que são empregadas técnicas cada vez mais sofistica- das. Além disso, o estudo das relações de parentesco entre os organismos, como proposto pelo entomologista alemão Willi Hennig, tem motivado os biólogos a reviver a anatomia por ser ela indicativa das relações entre os táxons. Assim, as novas idéias e os conceitos da sistemática filogenética foram, tam- bém, incorporados à ornitologia. Na década de 1980 iniciamos, na Universidade de São Paulo, um pro- grama de pesquisa com vários projetos em ornitologia que não haviam sido, até então, explorados no Brasil, voltados, principalmente, para a avifauna Neotropical. O novo grupo de pesquisa em anatomia conta, atualmente, com 18 pesquisadores e estudantes que trabalham nos seguintes temas: a) anatomia osteológica e miológica, que fornece subsídios para entender a mecânica dos movimentos, além de ser uma importante fonte de caracteres para sustentar hipóteses filogenéticas; b) anatomia da siringe, que tem pos- sibilitado a caracterização dos padrões morfológicos de vários grupos de aves; e c) pesquisa sobre aves fós- seis da América do Sul. Os táxons estudados nesses projetos pertencem principalmente às seguintes ordens: Tinamiformes, Ciconiiformes, Falconiformes, Galliformes, Opisthocomiformes, Gruiformes, Psittaciformes, Cuculiformes, Strigiformes, Trogoniformes, Coraciiformes, Piciformes e Passeriformes (i.e., Furnariidae e Dendrocolaptidae).

Abstract. – The knowledge of anatomy is a necessary prerequisite for understanding changes in charac- ters, and the evolutionary history of organisms. Traditional methods of anatomical study have been gradu- ally replaced by functional and dynamic approaches, using techniques that have become increasingly sophisticated over time. Moreover, the study of the relationships among organisms, as proposed by the German entomologist Willi Hennig, has motivated biologists to revive anatomy as the basic indicator of biological relationships among taxa. Ornithology has kept pace with these new ideas and concepts. In the early ’80s, at the Universidade de São Paulo, we began a research program with various ornithology projects on aspects that had not been previously explored in Brazil, and that focused on the Neotropical avifauna. This anatomical research group currently consists of 18 scientists and students working on the following topics: a) osteological and myological anatomy, which enables us to understand the mechanics of movement and provides with a series of important characters to support phylogenetic hypotheses; b) the anatomy of the syrinx, which is important for the characterization of morphological patterns of various groups; c) research on the fossil avifauna of South America. The taxa studied in all these projects belong mainly to the following orders: Tinamiformes, Ciconiiformes, Falconiformes, Galliformes, Opis- thocomiformes, Gruiformes, Psittaciformes, Cuculiformes, Strigiformes, Trogoniformes, Coraciiformes, Piciformes, and Passeriformes (i.e., Furnariidae and Dendrocolaptidae). Accepted 9 December 2003.

Key words: Anatomy, systematics, Brazil, phylogenetic hypotheses, fossil birds.

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In Latin America there are relatively few avian sidered a morphologically uniform group of anatomists. In Brazil, I have the privilege of vertebrates. belonging to this select group, together with Whereas the ecology, behavior and repro- my current and former students of the last ductive biology of birds received increasing two decades. We worked mainly with extant attention, particularly during the second half birds, but more recently we included some of the 20th century, the anatomy of birds was fossil taxa. In Argentina, avian anatomists are neglected and little effort was made to absorb represented mainly by paleontologists with at modern concepts of comparative biology least five active researchers working on fossil therein. Perhaps this was partly because orni- birds. thology began to adopt the concepts of phy- logenetic reconstruction, notably the cladistic approach, only relatively late among zoologi- HISTORIC OVERVIEW OF AVIAN cal disciplines. In addition, the power of the MORPHOLOGY evolutionary school in ornithology is seen in the frequent use of trinomials (i.e., subspe- One cannot talk about anatomical studies cies). This concept was much used by orni- without acknowledging the pioneer contribu- thologists, despite its conceptual incons- tions made in this area especially during the th istencies (de Pinna 1999), and Cracraft second half of the 19 century, which was an (1974, 1981, 1988) was the one who pio- extremely important and fertile period for neered the use of cladistic methods in orni- bird anatomy. At that time, classical studies thology. were produced e.g., by Blanchard (1859), Gar- Birds are frequently considered to be a rod (1873a, 1873b, 1874), Fürbringer (1888), morphologically homogeneous group, at least Seebohm (1888, 1895), Gadow (1889, 1892), in comparison to other vertebrates. Neverthe- and Beddard (1898). The first proposals for less, this homogeneity is only relative and avian classifications were established by should not be considered as an impediment grouping birds based on total similiarities of attempts to identify characters with phylo- within a precladistic philosophy. The classical genetic information. On the contrary, we work of Beddard (1898), entitled “The struc- should increase research in this area, and sev- ture and classification of birds”, assumed an eral studies show that morphological charac- important role in ornithology, not only ters exist and are informative (Livezey & Zusi because of the quality of anatomical descrip- 2001). tions, but also because of its taxonomic With the advance of molecular biology scope. since 1990, a new discipline started in orni- Stresemann (1959) considered that the thology. Several molecular studies have pro- relationships among the large groups of birds vided new phylogenetic hypotheses for avian were so well established that any newly dis- taxa. Works based on molecular data have covered species could simply be assigned to assumed a dominant role in systematics due one of these groups. This statement contrib- to the large amount of information derived uted to the belief, which has predominated in from DNA, and due to technical advances in ornithology until very recently, that little the extraction, sequencing, and analysis of the remains to be done in bird anatomy and sys- DNA molecule. However, the large amount tematics. Partly as a consequence of this view, of base-pair does not necessarily represent suprageneric systematics advanced only data that contain phylogenetic information. slowly during a time in which birds were con- Thus, analyses of molecular data should be

74 AVIAN ANATOMICAL STUDIES integrated together with anatomical and other migration, molecular biology and conserva- source of taxonomic data. A coherent matrix tion. In Brazil, over the last two decades, ana- of such data may help to eliminate the noise tomical studies focusing mainly on the generated by enormous quantities of molecu- Neotropical avifauna have been carried out by lar data, thereby permitting more trustworthy two research groups: one at the Universidade phylogenetic hypotheses using the total evi- Federal de Minas Gerais in Belo Horizonte dence of characters (e.g., Kluge 1989). led by Gérman A. B. Mahecha, and the other group at the Universidade de São Paulo. The NEOTROPICAL BIRDS first group has worked mainly on the repro- ductive apparatus of the Tinamidae as well as François Vuilleumier (2003) published an on other anatomical aspects, including histo- important review entitled “Neotropical Orni- pathology (Oliveira & Mahecha 1996, thology: then and now”. The reading of Mahecha & Oliveira 1998, Oliveira & this paper is recommended for anyone Mahecha 2000, Mahecha & Oliveira 2001, who wants to learn something about the his- Mahecha et al. 2002). The other group began torical development of our knowledge of studies in the early 1980s and has investigated Neotropical birds, and to receive suggestions the following topics: (1) osteological and myo- for future studies. Vuilleumier (2003) particu- logical anatomy, which enables us to under- larly emphasizes the fundamental role of sys- stand the mechanics of movement and tematics in ornithology, and, in this context, I provides a series of important characters to would like to stress that anatomy is a basic test phylogenetic hypotheses; (2) anatomy of tool for such studies. Livezey & Zusi (2001) the syrinx, which enables the characterization have noted that there is a large amount of of morphological patterns for various bird under-utilized anatomical information at our groups, even in spite of a low resolving power disposal in the literature, which implies that a at the species level; (3) research on the fossil potentially important source of characters birds of South America. with phylogenetic information has been neglected for decades and should be Comparative anatomy and systematics. Our reclaimed. descriptive osteological and myological study Various researchers (e.g., Olson 1983, of the skull and jaw apparatus of toucans, Raikow & Cracraft 1983, Burton 1984, Prum including the aponeuroses of each muscular 1988, Cracraft & Prum 1988) have used Neo- band (Höfling & Gasc 1984a), formed the tropical avian taxa in their surveys, thus basis for the kinetic analysis of the skull in this enriching the base for systematics and evolu- group (Höfling & Gasc 1984b). In species of tionary studies of birds. But anatomy also has the Ramphastos, there is a sheet of con- an important role in clarifying our under- nective tissue that is continuous with the pos- standing of the function of structures, in the torbital ligament. Burton (1984), in contrast, area of biomechanics and functional anatomy, concluded that there is no postorbital liga- which applies the principles of classical ment in the Ramphastidae. However, mechanics to living , including birds. although this is true for species of other ram- In Latin America, few people have dedi- phastid genera, it is not the case with Rampha- cated themselves to anatomical studies, stos, which does have such a ligament. This although there has been considerable devel- example highlights the dangers of generalizing opment in ornithology in other areas, such as characters for all members of a family. We can ecology, behavior, reproductive biology, consider the presence of the postorbital liga-

75 HÖFLING ment as an important mechanical trait for the based on molecular data proposed by Pereira larger species, and as a diagnostic character et al. (2002). This disagreement indicates the for the genus Ramphastos. need for further research with a larger sample Several groups of Neotropical birds have of characters. been studied for cranial and myological char- As noted by Zusi (1993), the ontogenetic acteristics that may be used to interpret sys- development of the skull also furnishes tematic relationships. These groups are the important data for identifying homologies, following: Galbulidae (Donatelli 1992), since the adult skeleton alone may offer insuf- Picidae (Donatelli 1996), Opisthocomidae ficient data for phylogenetic hypotheses. (Marceliano 1996), Psophiidae (Donatelli et al. When there are juveniles available for study, 1997), Dendrocolaptidae (Donatelli 1997), which is rare, such a comparative approach Cuculidae (Posso 1999, Posso & Donatelli may be productive, as we can see in the Tina- 2001), Bucconidae (Alvarenga et al. 2002 midae (Silveira & Höfling in press). Ladeira & Höfling in press), Momotidae (Pas- A comparative study of the morphometric cotto & Donatelli 2003), Cracidae (Silveira characteristics of the skull (Höfling 1991, 2003, Silveira & Höfling 2003), Tinamidae 1995), analyzed 33 skull measurements of 19 (Silveira & Höfling in press), and Alcedinidae species of Ramphastidae, and showed that (Mendez & Höfling in press). certain measurements, such as the length and Silveira & Höfling (2003) analyzed the caudal width of the skull, have a low coeffi- complete skeletons of 44 out of 50 recog- cient of variation, whereas others, such as the nized species of Cracidae and of 25 species upper maxilla, have a high one. Morphomet- from 14 genera as the outgroup. On the basis ric analysis of the braincase shows that ram- of this analysis, they established the validity of phastid species are very conservative with 151 characters. A phylogenetic analysis gener- regard to these measuments. Another aspect ated a very robust cladogram that showed: (a) observed in a sample of 84 specimens of the existence of two subfamilies, the Cracinae these 19 species was the intraspecific mor- and the Penelopinae, which supports the orig- phological variation of the fronto-nasal inal classification by Huxley (1868); (b) the suture. subfamily Cracinae is composed of the genera In general, the skull does not provide sig- Nothocrax, Pauxi, and Crax, whereas the gen- nificant interspecific anatomical differences. era Oreophasis, Penelopina, Aburria, Penelope, Nevertheless, we were able to validate Nothar- Chamaepetes, and Ortalis belong to the subfam- chus swainsoni (Gray, 1846), a puffbird from ily Penelopinae; (c) there is no support for southeastern Brazil, Paraguay, and northeast- maintaining the genera Pipile Bonaparte, 1856, ern Argentina, by craniological differences in and Mitu Lesson, 1831, but rather the analysis addition to the characteristics of plumage indicates that these genera should be consid- color, size, and geographical distribution ered synonymous with Aburria Reichenbach, (Alvarenga et al. 2002). In osteology, the main 1853, and Pauxi Temminck, 1813, respec- differences are in the width and shape of the tively, which results in the reduction of the temporal fossae, in the opening between the genera from eleven to nine; (d) osteology, in palatines, and in the thickness and height of the Cracidae, does not provide characters that the maxillary processes of the nasals. can be used unequivocally to define the rela- An osteological study of the shoulder gir- tionships among species belonging to the dle of the Piciformes, Coraciiformes, Passeri- same genus. This cladogram based on mor- formes and other related groups, such as the phological data is very different from that Trogoniformes, Coliiformes, Apodiformes,

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Strigiformes and Caprimulgiformes (Höfling Gasc 1994), it was possible to verify, that & Alvarenga 2001), permitted a re-evaluation depending on the extent of the mandibular of their systematic relationships. A number of depression (between 22° and 25.8°), the observed characters justify the inclusion of upper jaw is elevated relative to the braincase the families Indicatoridae, Picidae, Capi- between 5.5° and 6.7° in Ramphastos toco and tonidae, and Ramphastidae in the Piciformes. 3.8° in R. vitellinus, but that such a movement Furthermore, the characters indicate that (a) is practically absent in R. dicolorus. the Piciformes and Passeriformes have a Currently, we are working on the terres- monophyletic origin; (b) the Galbuloidea, trial locomotion of Neotropical birds based including the Galbulidae and Bucconidae, on film analyses of Tinamidae and Cariamidae should not be placed in the Piciformes (Abourachid et al. 2003), comparing walking because they are closer to the Coraciiformes, kinematic parameters between paleognathous both groups possessing a developed procora- and neognathous birds. coid process; and (c) the Trogonidae and Coraciiformes are not related. South American fossil birds. A knowledge of Some undergraduate and graduate stu- anatomy is a fundamental tool for fossil bird dents are currently studying the syringeal studies, and we can deduce several character- anatomy for phylogenetic purposes, although istics for an individual that lived some millions it is necessary to use a large series of speci- of years ago from one or a few fossilized mens, because this organ presents enormous bones. For example, the first bird from the intraspecific variation. The first study, dealing Tertiary of Chile, Meganhinga chilensis, was a with 25 species (105 specimens) of New large and probably flightless anhinga, whose World parrots (Gaban-Lima 2001, Gaban- holotype was designated by its tarsometatar- Lima & Höfling 2002), showed that we can sus, even though there were several other identify three patterns of variation in the bones from at least two individuals available syringeal anatomy of Arini: chaotic intraspe- (Alvarenga 1995). The South American, in cific variation, intraspecific variation with a particular Brazilian, fossil birds were reviewed discernible pattern among taxa, and interspe- by Alvarenga & Höfling (2000), but several cific variation (fixed characters). However, in additional South American fossil birds have the genus Xiphorhynchus (Raposo 2001), as in been described since that publication (Olson some dendrocolaptid genera (Raposo et al. in & Alvarenga 2002, Alvarenga & Guilherme prep.), the syringeal anatomy does not help in 2003, Alvarenga & Olson 2004). species characterization. The systematic revision of the Phorusrha- cidae (Alvarenga & Höfling 2003) is an exam- Biomechanics and functional anatomy. With regard ple of such studies. Throughout the Tertiary, to functional anatomy, the cranial kinesis and South America was inhabitated by these ralli- the locomotion of Neotropical birds have form birds. The are amongst been studied. Höfling & Gasc (1984b) dis- the largest birds that have ever existed, and cussed several aspects of such functional anal- burmeisteri is the largest phorusrha- yses in the genus Ramphastos. With the cid and the largest known bird of the Ameri- particular specimens studied and the particu- can continent, reaching more than 250 cm in lar type of analysis employed at that time we height and weighing more than 400 kg. The could not verify the prokinesis of the skull. limited number of known specimens of Bron- Subsequently, with additional specimens and tornis burmeisteri does not allow for more pre- different analytical techniques (Höfling & cise calculations. The skeleton of the only

77 HÖFLING known specimen of brasiliensis Museu de História Natural de Taubaté Alvarenga, 1982, was re-constructed and con- (MHNT) has the most representative and well sidered to have been around 240cm high. The prepared collection of skeletons (about 2000) femora and tibiotarsi of this bird have much and fossil birds. In Argentina, at the Museo larger diameters and circumferences than de La Plata, there are two skeleton collections those of a large male specimen of an ostrich (about 350). The Museo Argentino de Cien- (Struthio camelus) with a live body-mass of 130 cias Naturales “Bernardino Rivadavia” has kg. This indicates that the weight of Paraphys- approximately 200 skeletons, and the Centro ornis brasiliensis may have been around 180 kg. de Investigationes Cientificas y Transferencia The smallest phorusrhacid, Psilopterus bach- de Tecnología a la Producción, in Diamante, manni, was had approximately the same height has about 100 skeletons. (i.e., about 80 cm) as the present-day Seriema As Zusi (1993) suggested, advances in (Cariama cristata), and weighed nearly 5 kg. anatomical research will ultimately depend on the availability of anatomical specimens. ANATOMICAL COLLECTIONS Worldwide inventories of anatomical speci- mens make it possible to be selective and effi- In Latin America, anatomical collections of cient in developing our collections for the birds have been neglected as a whole, and maximum benefit to science (Zusi et al. 1982, there were no criteria or incentives to build Wood & Schnell 1986). The prospects for some. Skeleton collections were established anatomical research on Neotropical birds are mainly in those places where paleontologists very promising. were working, as the Museo de La Plata in We have a dream: to see anatomical stud- Argentina, and at the Museu de História Nat- ies established and diffused in Latin America ural de Taubaté in Brazil. Alvarenga (1992) equal to the other areas of ornithology. has drawn attention to the role of osteological Unfortunately, some ornithologists have not collections for Brazilian ornithology. Few yet recognized the fundamental value of institutions in South America possess a repre- anatomy for ornithological systematics and sentative anatomical collection. The Museu phylogenetic hypotheses, as well as for under- Paraense Emilio Goeldi (MPEG) has a good standing the evolution of present and past anatomical collection of Amazonian species avifauna of the Neotropical region. preserved in alcohol (around 8400 specimens) and also a skeleton collection composed ACKNOWLEDGMENTS mainly of skulls (around 4000 specimens). In the Museu Nacional do Rio de Janeiro I dedicate this article to my former and cur- (MNRJ), there is a small anatomical collection rent students who are spreading anatomical with few prepared skeletons. Around a thou- research to various Brazilian institutions and sand of anatomical specimens (some 400 skel- universities. They believe that bird anatomy is etons and 600 specimens in alcohol) are a rich discipline with interesting problems to available at the Museu de Zoologia da Univer- be studied, and with many questions to be sidade de São Paulo (MZUSP). The Departa- answered. I thank H. M. F. Alvarenga, L. F. mento de Zoologia do Instituto de Silveira, P. Gibbs and D. Homberger for criti- Biociências da Universidade de São Paulo cal reading of the manuscript. I also thank the (AZ) has a very specific collection linked to Conselho Nacional de Desenvolvimento our anatomical research (around 200 skele- Científico e Tecnológico (CNPq) and the tons and 550 specimens in alcohol). The Fundação de Amparo à Pesquisa do Estado

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