The Phylogenetic Affinities of the Shoebill (Balaeniceps Rex) Gerald Mayr

Home , Ardei, Balaenicipitidae, Hamerkop, Shoebill

J. Ornithol. 144, 157±175 (2003) ã Deutsche Ornithologen-Gesellschaft/Blackwell Verlag, Berlin ISSN 0021-8375

The phylogenetic affinities of the Shoebill (Balaeniceps rex) Gerald Mayr

Forschungsinstitut Senckenberg, Sektion fuÈr Ornithologie, Senckenberganlage 25, D-60325 Frankfurt/M., Germany; E-mail: [email protected]

Summary The phylogenetic affinities between the shoebill (Balaenicipitidae) and pelecaniform and ciconiiform birds are analysed. A cladistic analysis of 54 anatomical characters resulted in monophyly of the taxon (Scopidae + (Balaenicipitidae + Steganopodes (sensu Cracraft 1985))) and showed both Ciconiiformes and Pelecaniformes to be polyphyletic. Derived characters which support the resulting phylogeny are discussed. Monophyly of the taxon (Scopidae + (Balaenicipitidae + Steganopodes)) is better supported by morphological evidence than monophyly of the taxon (Procellariiformes + (Phaethontidae + Steganopodes)) which was established by Cracraft (1985). The shared derived characters of Scopidae, Ba- laenicipitidae and Steganopodes are furthermore less easily explained by convergent evolution than by the few characters which support monophyly of the taxon (Phaethontidae + Steganopodes). The Phaethontidae share derived characters with the Procellariiformes, which might support a sister group relationship between the two taxa.

Keywords: Phylogeny, Balaenicipitidae, Scopidae, Pelecaniformes, Ciconiiformes, Procellarii- formes, osteology.

Zusammenfassung Die phylogenetischen Beziehungen des Schuhschnabels (Balaeniceps rex) Die phylogenetischen Beziehungen zwischen dem Schuhschnabel (Balaenicipitidae) und pelecaniformen und ciconiiformen VoÈgeln werden untersucht. Eine kladistische Analyse von 54 anatomischen Merkmalen resultierte in Monophylie des Taxons (Scopidae + (Ba- laenicipitidae + Steganopodes (sensu Cracraft 1985))) und ergab, dass sowohl Ciconiifor- mes als auch Pelecaniformes polyphyletisch sind. Abgeleitete Merkmale, welche den resultierenden Stammbaum begruÈnden, werden diskutiert. Monophylie des Taxons (Sco- pidae + (Balaenicipitidae + Steganopodes)) ist besser gestuÈtzt durch morphologische Merkmale, als die von Cracraft (1985) begruÈndete Monophylie des Taxons (Procellariifor- mes + (Phaethontidae + Steganopodes)). Die gemeinsamen abgeleiteten Merkmale von Scopidae, Balaenicipitidae und Steganopodes lassen sich daruÈber hinaus weniger leicht durch Konvergenz erklaÈren, als die wenigen Merkmale, welche Monophylie des Taxons (Phaethontidae + Steganopodes) begruÈnden koÈnnten. Die Phaethontidae teilen abgeleitete Merkmale mit den Procellariiformes, welche eine Schwestergruppenbeziehung zwischen beiden Taxa stuÈtzen koÈnnten.

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Introduction the columella (ear ossicle). Cracraft (1981, 1985, 1988) also regarded the similarities be- The shoebill (Balaeniceps rex) is the sole liv- tween Balaeniceps and pelicans as convergen- ing representative of the Balaenicipitidae and ces and assumed that the shoebill was the sister today only occurs in remote swamps of east- taxon of herons. Cracraft (1985) performed a central Africa. It is a fairly rare and, despite its cladistic analysis of the Pelecaniformes in popular appeal in zoological gardens, rather which he also included the shoebill but no ci- poorly studied solitary bird which feeds on coniiform birds. Rea (1983) considered Balae- fishes and small vertebrates (see Elliott 1992). nicipitidae, Scopidae, Threskiornithidae, Cico- Although it is generally classified within the niidae and Cathartidae (New World vultures) Ciconiiformes, together with storks (Ciconii- to be closely related. A cladistic analysis of dae), herons (Ardeidae), ibises (Threskiorni- characters of the hind limb musculature by thidae) and the hamerkop (Scopidae) (del McKitrick (1991) resulted in monophyly of Hoyo et al. 1992), there is no consensus about Balaenicipitidae and Ardeidae, and these two the phylogenetic affinities of the shoebill. taxa were widely separated from other ciconiiform and from pelecaniform birds (the Scopi- Gould (1852) regarded Balaeniceps as an dae were not included in the analysis which aberrant pelican, but subsequent authors espe- yielded several very unlikely results as, for ex- cially noted morphological similarities to ample, paraphyly of ducks and geese, Anati- herons (Bartlett 1861, Parker 1861, Beddard dae). Mikhailov (1995), on the other hand, in- 1888, Gadow 1893) and the African hamer- vestigated the eggshell microstructure of the kop, Scopus umbretta (Reinhardt 1861, Giebel shoebill and found derived similarities to that 1873). BoÈhm (1930) thought that Balaeniceps of Scopus and most pelecaniform birds. An was more closely related to storks than to analysis of 20 morphological characters by herons but did not make comparisons with Siegel-Causey (1997) showed a taxon includ- Scopus. The idea of a closer affinity between ing Balaenicipitidae, Fregatidae and Pelecani- Balaenicipitidae and pelecaniform birds was dae to be monophyletic; the corresponding revived by Cottam (1957) who, curiously, also clade received, however, weak bootstrap sup- omitted Scopus from her comparisons because port and the analysis was mainly restricted to ªthere is no point in comparing one genus of pelecaniform taxa. A cladistic analysis of char- doubtful affinities with anotherº; for the same acters of the skull and the vertebral column by reason she did not make comparisons with the Livezey & Zusi (2001) resulted in monophyly pelecaniform Phaethontidae. Cottam (1957) of Balaenicipitidae and Pelecanidae (pelicans); did not clearly state to which pelecaniform characters supporting the resulting phylogeny taxon she considered Balaeniceps to be most were, however, not given and the results of this closely related, but indicated that it should be study were explicitly considered by the authors placed ªpossibly near the Pelecanidaeº. On the to be preliminary. basis of a study of the middle ear region Saiff (1978) also concluded that the shoebill was In recent years, several molecular studies more closely related to pelecaniform than to have addressed the relationships between Ba- ciconiiform birds, and Olson (1979) noted that laeniceps and pelecaniform birds. The results ªit appears possible that the Balaenicipitidae, of their DNA-DNA hybridisation studies led Scopidae and Ciconiidae may represent a more Sibley & Ahlquist (1990) to include Balaeni- or less natural assemblage having affinities ceps in the Pelecanidae. An analysis of DNA- with the Pelecaniformesº. However, Feduccia DNA hybridisation data and mitochondrial (1977) thought that the Balaenicipitidae were DNA sequences by Hedges & Sibley (1994) the sister taxon of the Ciconiidae because both also resulted in monophyly of the taxon (Ba- taxa shared a similar derived morphology of laenicipitidae + Pelecanidae), as did an analy- G. Mayr ´ Shoebill phylogeny 159 sis of mitochondrial and cytochrome b sequen- from the Oligocene of Egypt (Rasmussen et al. ces by Siegel-Causey (1997) (Fig. 1). An ana- 1987) and the Miocene of Tunisia and Pakistan lysis of DNA-DNA hybridisation data, as well (Harrison & Walker 1982), which do not con- as nuclear and mitochondrial DNA sequences tribute to an understanding of the affinities of by van Tuinen et al. (2001) supported mono- these birds. Assessment of the phylogenetic phyly of the taxon (Scopidae + (Balaenicipiti- position of the Balaenicipitidae is further dae + Pelecanidae)) (Fig. 1). obscured by the fact that neither monophyly The fossil record of the Balaenicipitidae is of the traditional Ciconiiformes (as defined very poor and consists of fragmentary remains above) nor of the Pelecaniformes, i. e. a clade

Fig. 1. Recent hypotheses on the phylogenetic relationships of the Balaenicipitidae in comparison. The phylogenies are based on analyses of morphological characters (Cracraft 1985), DNA sequences of the mitochondrial 12S rRNA and 16S rRNA genes (Hedges & Sibley 1994), DNA sequences of the mitochondrial 12S rRNA and 16S rRNA genes and cytochrome b nucleotide sequences (Siegel-Causey 1997), and DNA sequences of the c-mos proto-oncogene exon, G3PDH intron 11, and complete 12S rRNA, tRNAVal and 16S rRNA genes (van Tuinen et al. 2001). Abb. 1. Neuere Hypothesen uÈber die Verwandtschaftsbeziehungen der Balaenicipitidae im Vergleich. Die StammbaÈume basieren auf Analysen morphologischer Merkmale (Cracraft 1985), DNA-Sequenzen mitochondrieller 12S rRNA- und 16S rRNA-Gene (Hedges & Sibley 1994), DNA-Sequenzen mitochondrieller 12S rRNA- und 16S rRNA-Gene und Cytochrom-b-Nukleotid-Sequenzen (Siegel-Causey 1997), sowie DNA-Sequenzen des c-mos proto-oncogene exon, des G3PDH intron 11 und vollstaÈndiger 12S rRNA-, tRNAVal- und 16S rRNA-Gene (van Tuinen et al. 2001). 160 Journal fuÈr Ornithologie 144, 2003 including Phaethontidae (tropicbirds), Fregati- procellariiform Pelecanoididae unfortunately were dae (frigatebirds), Pelecanidae (pelicans), Su- not available for study. lidae (boobies and gannets), Phalacrocoracidae Most non-osteological characters were taken (cormorants) and Anhingidae (darters), has from the literature. Anatomical terminology follows been conclusively established (see Sibley & Baumel & Witmer (1993) and Vanden Berge & Ahlquist 1990 and discussion below). The Zweers (1993), if not otherwise indicated. Follow- present study is the first cladistic analysis of ing Cracraft (1985), the term Steganopodes is used the phylogenetic relationships of Balaeniceps for the taxon including Fregatidae, Pelecanidae, Su- to cover a wide range of morphological data, lidae, Phalacrocoracidae and Anhingidae. includes representatives of all ciconiiform and A phylogenetic analysis with the cladistic soft- pelecaniform families, and lists the derived ware PAUP, version 3.1 (Swofford 1993) was per- characters which support the resulting phylog- formed on a data set of 54 anatomical characters eny. (see Appendices for character descriptions and character matrix). Two characters were coded as ªor- deredº. The shortest tree was found with the ªbranch-and-boundº search option and the analysis Material and methods was run in the accelerated transformation (AC- CTRAN) mode. The consistency index (CI), reten- Skeletons of the following taxa were examined in tion index (RI) and rescaled consistency index (RC) the collection of the Forschungsinstitut Senckenberg were calculated and the robustness of the tree was and of the UniversiteÂ Claude Bernard, Lyon: Tina- tested with a bootstrap analysis of 1000 replicates. midae: Crypturellus cinnamomeus, C. obsoletus, Most behavioural characters included in the ana- C. parvirostris, C. undulatus, Nothura boraquira, lysis of Cracraft (1985) were omitted from this study Rhynchotus rufescens, Tinamus solitarius. Ardei- because homology with similar behavioural patterns dae: Agamia agami, Ardea cinerea, A. goliath, in pelecaniform, procellariiform and ciconiiform A. herodias, A. purpurea, Ardeola grayii, A. ral- birds in many cases is uncertain (van Tets 1965). loides, Botaurus stellaris, Butorides striatus, Coch- Outgroup comparisons were made with the palaeog- learius cochlearius, Egretta alba, E. garzetta, nathous Tinamidae, which are generally considered E. gularis, E. sacra, E. thula, Ixobrychus minutus, to be the sister taxon of neognathous birds (Groth & Nycticorax nycticorax. Scopidae: Scopus umbretta. Barrowclough 1999, Livezey & Zusi 2001). Balaenicipitidae: Balaeniceps rex. Ciconiidae: Anastomus lamelligerus, Ciconia abdimii, C. ciconia, C. nigra, Leptoptilos crumeniferus, Mycteria Results ibis, M. leucocephala. Threskiornithidae: Eudoci- mus ruber, Geronticus eremita, Hagedashia hage- Results of the phylogenetic analysis with dash, Lophotibis cristata, Platalea ajaja, P. alba, PAUP 3.1 P. leucorodia, Plegadis falcinellus, Threskiornis aethiopicus, Th. melanocephala. Phaethontidae: Analysis of the character matrix in Appen- Phaethon cf. lepturus (subfossil bones). Fregatidae: dix II with PAUP 3.1 resulted in ten most par- Fregata spec.. Pelecanidae: Pelecanus occidentalis, simonious trees, the consensus tree of which is P. onocrotalus, P. rufescens. Sulidae: Sula bassana, shown in Fig. 2B. This analysis supported S. sula, S. cf. dactylatra. Phalacrocoracidae: Phala- monophyly of the taxon (Scopidae + (Balaeni- crocorax aristotelis, Ph. auritus, Ph. carbo, Ph. gai- cipitidae + Steganopodes)) which received a mardi, Ph. harrisi, Ph olivaceus (skull), Ph. penicil- bootstrap support of 73 %. Monophyly of the latus. Anhingidae: Anhinga anhinga. Diomedeidae: taxon (Balaenicipitidae + Steganopodes) re- Diomedea melanophrys. Procellariidae: Bulweria bulwerii, Calonectris diomedea, Daption capensis, ceived a weak bootstrap support of 56 %, Fulmarus glacialis, Macronectes giganteus (skull), monophyly of the Steganopodes did not re- Procellaria aequinoctialis, Pterodroma hypoleuca, ceive any bootstrap support. In seven of the P. neglecta, Puffinus puffinus. Hydrobatidae: Oce- resulting trees, the Pelecanidae are the sister anodroma castro, O. leucorhoa. Specimens of the group of the clade (Sulidae + Phalacrocoraci- G. Mayr ´ Shoebill phylogeny 161

Fig. 2. A: The phylogeny proposed in this study; derived characters supporting the numbered nodes are listed in the text. B: Consensus tree of ten most parsimonious trees resulting from an analysis of the character matrix in Appendix II with PAUP 3.1 (Length = 126, CI = 0.48, RI = 0.52, RC = 0.30); the bold values indicate the bootstrap support of the respective nodes (1000 replicates, see also text). Abb. 2. A: Der hier vorgestellte Stammbaum; abgeleitete Merkmale, welche die nummerierten Verzwei- gungspunkte stuÈtzen sind im Text aufgefuÈhrt. B: Konsensus-Stammbaum von zehn aus der Analyse der Merkmalstabelle in Anhang II mit PAUP 3.1 resultierenden sparsamsten StammbaÈumen (LaÈnge = 126, CI = 0.48, RI = 0.52, RC = 0.30); die fettgedruckten Ziffern geben die Bootstrap-Werte an (1 000 Wiederho- lungen, siehe Text).

dae/Anhingidae), in three trees the Fregatidae Monophyly of Scopidae, Balaenicipitidae and are the sister taxon of this clade, which is, Steganopodes (Fig. 2A, node 1) however, supported by a single derived charac- Monophyly of Scopidae, Balaenicipitidae and ter only (character 53 in Appendix I; other the Steganopodes (Fregatidae, Pelecanidae, characters were optimised as derivative rever- Sulidae, Phalacrocoracidae and Anhingidae) is sals into the primitive state). The clade includ- supported by the following derived characters ing Pelecanidae, Sulidae, Phalacrocoracidae (the numbers refer to Appendix I): and Anhingidae was retained in the bootstrap analysis and got a support of 61 %. The Phae- (1) Upper beak, praemaxilla with sharply thontidae were optimised as sister taxon of the hooked tip (Fig. 3). Since the diet of the hamer- Procellariiformes in nine of the resulting trees, kop does not significantly differ from that of in one tree their position was unresolved; boot- storks and herons, the presence of a hooked strap analysis did not support sister group praemaxilla appears to be of phylogenetic relationship between Phaethontidae and Pro- rather than functional significance. The ab- cellariiformes. sence of this character in the Anhingidae and its weak development in the Sulidae is here In contrast to the studies of Cracraft (1985: considered to be due to the highly derived feed- therein Fig. 6, 7, 8B) and Siegel-Causey ing technique of these birds (see Appendix I). (1997: therein Fig. 6.2), monophyly of the Pro- (4) Upper beak, praemaxilla with marked cellariiformes (Hydrobatidae, Procellariidae furrow distal of nasal opening (Fig. 3). The ab- and Diomedeidae) was highly corroborated sence of this character in the Anhingidae is with a bootstrap value of 93 %. here considered autapomorphic for that taxon 162 Journal fuÈr Ornithologie 144, 2003

Fig. 3. Skull in comparison. A, Balaeniceps rex (Balaenicipitidae); B, Scopus umbretta (Scopidae). The arrows indicate the marked furrow distal of the nasal opening. Note to Scale. Abb. 3. SchaÈdel im Vergleich. A, Balaeniceps rex (Balaenicipitidae); B, Scopus umbretta (Scopidae). Die Pfeile markieren die deutliche Rinne distal der NasenoÈffnung. Nicht im selben Maûstab. and is probably connected with the unique obliterated by fusion with clavicle)º. Accord- feeding technique of these birds (see Appen- ing to my observations, the fac. art. clavi- dix I). cularis is also strongly protruding in owls (5) Skull, ossified septum nasale present. (Strigidae), hawks (Accipitridae) and falcons This character does not occur in other puta- (Falconidae), but in these taxa its shape is dif- tively related taxa. ferent from that in the above-listed taxa. The (10) Skull, ossa palatina fused along their condition of this character in the Fregatidae midline. This character is found in few other needs further study (see Appendix I). unrelated taxa, e. g. toucans (Ramphastidae), (28) Sternum, dorsal surface with numerous hornbills (Bucerotidae) and frogmouths (Po- pneumatic foramina along midline and lateral dargidae) (not to be confused with the desmog- margins (Fig. 5). The absence of this character nathous palate in which the processus maxillo- in Phalacrocoracidae and Anhingidae is here palatini are fused). considered to be autapomorphic for these taxa; (22) Furcula, extremitas omalis with underlying the phylogeny in Fig. 2A, this as- strongly developed, laterally protruding facies sumption is more parsimonious than that of a articularis acrocoracoidea which articulates convergent origin of this character in Scopi- with a distinct ovoid facies articularis clavicu- dae, Balaenicipitidae, Fregatidae, Pelecanidae laris of the coracoid (Fig. 4). Olson (1984) and Sulidae. noted that the ovoid facies articularis clavicu- (38) Tarsometatarsus, hypotarsus with ten- laris of the coracoid distinguishes Scopus from don of musculus flexor digitorum longus and ªall other avian [taxa] except the Balaenicipi- m. flexor hallucis longus enclosed in bony ca- tidae and Pelecaniformes (within which the nal (Fig. 6). The absence of this character in Phaethontidae are exceptional in lacking this the Fregatidae, in which there is only a single character and the modern Fregatidae have it large canal for m. flexor digitorum longus, G. Mayr ´ Shoebill phylogeny 163 might be related to the fact that in frigatebirds birds) but rarely among the more basal Ne- the tarsometatarsus is extremely abbreviated. ornithes. In the Phalacrocoracidae there is only The tendons of both muscles are also enclosed a groove but no canal, which is here consid- in bony canals in several ªhigher land birdsº ered to be a derivative reversal into the primi- (e. g. most zygodactyl and some perching tive state.

Fig. 4. Furcula, right extremitas omalis in comparison. A: Balaeniceps rex (Balaenicipitidae); B: Scopus umbretta (Scopidae); C: Sula bassana (Sulidae); D: Agamia agami (Ardeidae, represents the primitive condition). The arrow indicates the strongly protruding facies articularis acrocoracoidea. Not to scale. Abb. 4. Furcula, rechte Extremitas omalis im Vergleich. A: Balaeniceps rex (Balaenicipitidae); B: Scopus umbretta (Scopidae); C: Sula bassana (Sulidae); D: Agamia agami (Ardeidae, primitiver Merkmalszustand). Der Pfeil markiert die weit hervorstehende Facies articularis acrocoracoidea. Nicht im selben Maûstab.

Fig. 5. Dorsal view of sterna in comparison. A: Balaeniceps rex (Balaenicipitidae); B: Scopus umbretta (Scopidae); C: Agamia agami (Ardeidae). The arrow indicates the pneumatic foramina along the midline. Not to scale. Abb. 5. Dorsalansicht des Sternums im Vergleich. A: Balaeniceps rex (Balaenicipitidae); B: Scopus umbretta (Scopidae); C: Agamia agami (Ardeidae). Der Pfeil markiert die pneumatischen OÈ ffnungen entlang der Mittellinie. Nicht im selben Maûstab. 164 Journal fuÈr Ornithologie 144, 2003

Fig. 6. Hypotarsus, proximal end in comparison. A: Balaeniceps rex (Balaenicipitidae); B: Sula bassana (Sulidae); C: Ciconia abdimii (Ciconiidae); D: Rhynchotus rufescens (Tinamidae, probably the primitive morphology of the hypotarsus). In A and B the tendons of musculus flexor digitorum longus and m. flexor hallucis longus are enclosed in bony canals. Not to scale. Abb. 6. Hypotarsus, proximales Ende im Vergleich. A: Balaeniceps rex (Balaenicipitidae); B: Sula bassana (Sulidae); C: Ciconia abdimii (Ciconiidae); D: Rhynchotus rufescens (Tinamidae, wahrscheinlich die primitive Morphologie des Hypotarsus). In A und B sind die Sehnen des Musculus flexor digitorum longus und des M. flexor hallucis longus von einem knoÈchernen Kanal umgeben. Nicht im selben Maûstab.

(41) Musculus expansor secundariorum morphology of the nasal cavity of Scopus and vestigial or completely absent. This muscle is the Steganopodes. also reduced in the Phaethontidae and a number of other taxa, none of which, however, Monophyly of Balaenicipitidae and seem to be closely related to the Balaenicipiti- Steganopodes (Fig. 2A, node 2) dae (Gadow 1891). Monophyly of Balaenicipitidae, Fregatidae, (54) Eggshell covered with a layer of mi- Pelecanidae, Sulidae, Phalacrocoracidae and croglobular material (amorphous form of cal- Anhingidae is supported by the following de- cium carbonate). This character is otherwise rived characters: known only from some herons, penguins (Spheniscidae) and some cuckoos (Cuculidae); (2) External narial openings greatly reduced in a few other taxa (Podicipediformes, Phoeni- or completely absent. In very few other avian copteriformes and the galliform Megapodii- groups are the external narial openings as dae) the layer consists of calcium phosphate greatly reduced as in the above-listed taxa. (Mikhailov 1995). In Balaeniceps and the (23) Furcula, apophysis furculae abutting Steganopodes the chalky covering of the egg is with an articular facet at the apex carinae of also macroscopically visible (Walters 1994). carina sterni (completely fused with the apex Characters (1), (4), (5), (10), (22) and (38) carinae in Balaenicipitidae, Pelecanidae and were also listed by Cottam (1957) as evidence Fregatidae). This character also occurs in the for the pelecaniform affinities of Balaeniceps. Ciconiidae. Technau (1936) further noted a great resem- This node received only weak bootstrap sup- blance in the position of the salt gland and the port in the analysis with PAUP 3.1 (Fig. 2B). G. Mayr ´ Shoebill phylogeny 165

Monophyly of Steganopodes to the exclusion Monophyly of Pelecanidae, Sulidae, of the Balaenicipitidae (Fig. 2A, node 3) Phalacrocoracidae and Anhingidae (Fig. 2A, node 4) Monophyly of the Steganopodes is supported by the following derived characters, none of Monophyly of Pelecanidae, Sulidae, Phalacro- which is present in Balaeniceps: coracidae and Anhingidae is in concordance (6) Conchae nasales greatly reduced or with most other studies of morphological data completely absent. This feature appears to be (Lanham 1947, Cracraft 1985) and is sup- unique to the Steganopodes; it is absent in the ported by: Phaethontidae (Technau 1936). (12) Vomer absent. (15) Recessus tympanicus dorsalis enlarged, situated rostrally or laterally to the ar- (27) Sternum, caudal portion of carina ster- ticular facets of the quadrate (Saiff 1978). ni reduced, apex carinae strongly cranially (44) Musculus flexor cruris lateralis, pars protruding. This character evolved conver- accessoria absent. This character occurs in gently in the Diomedeidae. several other avian taxa and certainly evolved (37) Tibiotarsus, distal end bent medially, several times independently (McKitrick 1991). condylus medialis protruding farther distally (47) Naked gular pouch present. than condylus lateralis. (50) Hallux included in webbed foot (48) Three anterior toes webbed over their (Fig. 7). This character otherwise only occurs entire length (Fig. 7). This character occurs in the Phaethontidae and is traditionally used in several other aquatic birds and certainly to define the Pelecaniformes (see discussion). evolved several times independently. (51) Young naked at hatching. This character is unquestionably derived in neornithine (52) Eggs incubated beneath feet. This birds but occurs in many other taxa. character is unique among extant birds.

Fig. 7. Feet in comparison (slightly schematic and not to scale). A: Phalacrocoracidae (cormorants); B: Fregatidae (frigatebirds); C: Phaethontidae (tropicbirds); D: Scopidae (hamerkop). Abb. 7. FuÈûe im Vergleich (leicht schematisch und nicht im selben Maûstab). A: Phalacrocoracidae (Kor- morane); B: Fregatidae (FregattvoÈgel); C: Phaethontidae (TropikvoÈgel); D: Scopidae (Hammerkopf). 166 Journal fuÈr Ornithologie 144, 2003

Monophyly of Sulidae, Phalacrocoracidae such as loons (Gaviidae) and grebes (Podicipe- and Anhingidae (Fig. 2A, node 5) didae). Monophyly of Sulidae, Phalacrocoracidae and (49) Hallux greatly reduced and consisting Anhingidae is supported by the following de- of a single phalanx only. rived characters: (11) Os palatinum an almost completely flat Discussion horizontal plate. This feature is unique among extant birds. Since virtually all of the derived characters (14) Processus paroccipitales protruding in shared by Scopidae, Balaenicipitidae and the caudal direction. Usually, these processes pro- Steganopodes (Fregatidae, Pelecanidae, Suli- ject ventrally. dae, Phalacrocoracidae and Anhingidae) are (16) Fossae temporales extending to mid- absent in the Phaethontidae, the position of the line of cranium. Usually these fossae are much Balaenicipitidae heavily depends on whether less developed. the traditional Pelecaniformes, i. e. the taxon (19) Quadratum, processus orbitalis re- comprising Phaethontidae and Steganopodes, duced. This feature is found in very few other are monophyletic. birds (e. g. parrots and swifts), none of which Cracraft (1988) listed 11 characters in order is closely related to the above-mentioned taxa. to support monophyly of the Pelecaniformes, Sulidae, Phalacrocoracidae and Anhingidae none of which, however, convincingly sup- further share a number of unique derived be- ports his hypothesis. The ªloss of supraorbital havioural similarities (van Tets 1965, Cracraft depressionsº (for the salt glands) clearly is 1985) and a derived number of 12 or 13 scleral primitive within neornithine birds (see below ossicles (Warheit et al. 1989). Monophyly of and Technau 1936), and the ªmediopalatine this taxon also is corroborated by virtually all processes [= crista ventralis]º are not ªanky- molecular analyses (Hedges & Sibley 1994, losed or fusedº in the Phaethontidae. The ªrel- Siegel-Causey 1997, Farris et al. 1999, van atively large ilio-ischiatic fenestraº is poorly Tuinen et al. 2001). defined and is not larger in the Fregatidae than, for example, in Scopidae and Balaenicipitidae. Monophyly of Procellariiformes A ªdeep, broad ligamental furrow of humerusº (Fig. 2A, node 6) occurs in many other neornithine taxa and is Monophyly of the Procellariiformes has not absent in the Pelecanidae and Sulidae (see Ap- been seriously questioned so far and is sup- pendices). The ªtotipalmate footº (hallux ported by the following derived characters: turned medially and all four toes connected by (3) External nostrils tubular. This feature is a web) is traditionally used to define the Pele- unique to the Procellariiformes. caniformes (Beddard 1898, Lanham 1947) but shows considerable variation within the taxon (17) Fossae glandulae nasales very marked in that the hallux is quite short in the Phaethon- and situated on dorsal surface of supraorbital tidae (long in the other pelecaniforms, as well margin of orbitae. as in Scopidae and Balaenicipitidae), and the (26) Coracoid, extremitas sternalis, proces- webbing is very rudimentary in the Fregatidae sus lateralis greatly elongated. (the web between the anterior toes is of similar (34) Humerus, large and strongly protrud- extension to that of, for example, the Scopidae; ing processus supracondylaris dorsalis present. see Fig. 7). Webbing of the three anterior toes (36) Tibiotarsus, proximal end, cristae cne- occurs in numerous unrelated avian taxa (e. g. miales strongly proximally protruding. This ducks, flamingos and gulls) and it is thus not feature is also found in other aquatic birds, unlikely that inclusion of the hallux into the G. Mayr ´ Shoebill phylogeny 167 web also evolved more than once (in penguins, ªpraeorbitalº position in the Sulidae, Phalacro- for example, the vestigial hallux is also turned coracidae, Anhingidae, Fregatidae and Scopi- medially and connected to the second toe dae (and in numerous other unrelated taxa such by an incipient web, see also Sibley & Ahl- as Columbidae, Podargidae and Coraciidae), quist 1990). The feathered ªgular pouchº of in an ªinterorbitalº position in the Pelecanidae the Phaethontidae is very inconspicuous (and and Ciconiidae (and others, such as Psittacidae might even not be present at all, see Sibley & and Strigidae), and in an ªinterorbital-exorbi- Ahlquist 1990); homology of this character talº position in the Phaethontidae (and others, within the Pelecaniformes was questioned by such as Caprimulgidae and Upupidae). The po- Sibley & Ahlquist (1990) and Siegel-Causey sition of the salt glands in pelecaniform birds (1997). The ªprelanding callº was first consid- thus appears to be of little phylogenetic value, ered to be a synapomorphy of the Pelecani- so much the less since Technau (1936) consid- formes by van Tets (1965) who noted that ered the ªpraeorbitalº position to be primitive. ªprobably all the Pelecaniformesº have a ªpre- Because of a greatly modified narial region, landing displayº. However, until this feature is the Balaenicipitidae lack salt glands (Technau better defined and its occurrence outside the 1936). Hedges & Sibley (1994) further stated Pelecaniformes is safely excluded, it also is of that all Pelecaniformes lack incubation questionable phylogenetic value. The ªrela- patches, but according to Orta (1992) in the tively horizontal preacetabular iliumº occurs Fregatidae these are even present in both pa- in many other avian taxa including Balaenici- rents. pitidae and Scopidae, the ªinternal condyle of Monophyly of the Pelecaniformes also is not tibio-tarsusº is ªgreatly enlarged relative to supported by any molecular analysis (Sibley & [the] externalº in almost all extant birds, and Ahlquist 1990, Hedges & Sibley 1994, Siegel- the ªgreatly foreshortened tarsometatarsusº is Causey 1997, van Tuinen et al. 2001). absent in the Pelecanidae and Phalacrocoraci- Cracraft (1985) further listed six characters dae (Cracraft 1985: tab. 1; moreover this bone in order to support monophyly of Procellarii- exhibits a completely different morphology in formes and Pelecaniformes to the exclusion of Phaethontidae, Fregatidae and Anhingidae). the Balaenicipitidae. However, again, none of The young also ªfeed by sticking heads down these characters is present in all pelecaniform gullet of adultº in penguins (Cracraft 1985) and procellariiform taxa: the ªmediopalatine and the young of many other birds at least in- processesº are not ªenlarged toward the ptery- troduce their beak into that of the adults when go-palatine jointº in the Fregatidae and Phala- being fed (van Tets 1965). Moreover, accord- crocoracidae (Cracraft 1985: tab. 1; since I ing to Howell (in Sibley & Ahlquist 1990), the found it difficult to code this character into dis- adults of the Fregatidae regurgitate food into crete character states, it is not included in the the throat of the young. present analysis); the ªupper tympanic recessº Sibley & Ahlquist (1990) and Hedges & Sib- [= recessus tympanicus dorsalis] is not ley (1994) added the position of the salt glands ªgreatly enlargedº in the Hydrobatidae and within the orbitae, on the ventral side of the some Procellariidae (see Appendices); the bo- supraorbital margin, as another possible syna- ny nostrils are not ªgreatly reducedº in the pomorphy of the Pelecaniformes. However, Phaethontidae and Procellariiformes (see Ap- the salt glands are not situated within the orbi- pendices); the rostrum of the Phaethontidae tae in the Phaethontidae (Technau 1936, Sie- lacks a ªlong nasal grooveº and a terminal gel-Causey 1990) nor do they share any de- hook (see Appendices); and the crista delto- rived similarities with the salt glands of the pectoralis (ªdeltoid crestº) of the humerus is Steganopodes (Technau 1936). According to not ªtriangular in shape and projecting to a Technau (1936) the salt glands are in a sharp pointº in the Hydrobatidae, Pelecanidae, 168 Journal fuÈr Ornithologie 144, 2003

Sulidae, Phalacrocoracidae and Anhingidae the Ciconiiformes as currently recognized (del (see Cracraft 1985 and Appendices). Hoyo et al. 1992) are polyphyletic and the Pro- The traditional (sensu del Hoyo et al. 1992) cellariiformes are not the sister taxon of the Ciconiiformes are even more poorly defined Pelecaniformes (contrary to Cracraft 1985). than the Pelecaniformes, since not a single Resolving the exact systematic position of the unique derived character has ever been pre- Phaethontidae was beyond the scope of this sented in order to show monophyly of this tax- study. Tropicbirds share several derived char- on. All characters listed by Beddard (1898) are acters with the Procellariiformes (e. g. the either plesiomorphic (e. g., ªoil gland feath- straight shaft and triangular crista deltopector- eredº, ªaftershaft presentº) or present in many alis of the humerus, and the complete webbing other taxa, including most Pelecaniformes of the anterior toes) but whether these similar- (e. g., desmognathous palate). Rea (1983) ities are indeed synapomorphic needs to be listed numerous characters in order to establish evaluated in a more comprehensive study a taxon including Balaenicipitidae, Scopidae, which also includes other taxa that were con- Threskiornithidae, Ciconiidae and Cathartidae sidered to be related to the Procellariiformes but did not distinguish between primitive and as, for example, penguins (Sibley & Ahlquist derived character states. He explicitly stated 1990). that his phylogenetic conclusions were based As detailed in the introduction, virtually all on ªoverall similarityº and in his long list I molecular analyses supported monophyly of could not find any derived character which the taxon (Balaenicipitidae + Pelecanidae), convincingly supports his classification (many which is not in concordance with the morpho- characters are present in virtually all neogna- logical evidence presented in this study. Mono- thous birds, e. g. ªfunctional primaries 10 or phyly of the shoebill and pelicans would imply 11º, others are clearly primitive and of no phy- either that the above-listed 11 derived charac- logenetic value, e. g. ªconspicuous gallbladder ters which, at two different hierarchical levels, presentº). Cracraft (1981) also considered the are shared by Pelecanidae, Sulidae, Phalacro- Ciconiiformes (in which he included the fla- coracidae and Anhingidae evolved independ- mingos) to be monophyletic but noted that the ently in pelicans or that they were secondarily supporting evidence is ªmore circumstantialº. reversed into the primitive condition in Balae- Citing Vanden Berge (1970), he mentioned a niceps (which, for example, does not show any single muscular character, the poor separation traces of webs between the toes). However, of musculus iliotrochantericus medius from m. most molecular studies were either based on iliotr. cranialis (ªanteriorº), in order to support the DNA-DNA hybridisation technique or his hypothesis. However, this character ap- used sequences of mitochondrial genes. The pears to be absent in at least some Ciconiidae methodology employed in DNA-DNA hybrid- (Vanden Berge 1970), is unknown for the Sco- ization studies is a comparison of ªmedian pidae (which were not investigated by Vanden similarity or dissimilarityº (Sibley & Ahlquist Berge 1970), and absent in Balaeniceps (Van- 1990) rather than a strict cladistic analysis of den Berge (1970) notes that in this taxon there derived characters and has for this reason been is a ªfairly definite line of separationº between criticised by several authors (Houde 1987, these muscles; see also Olson 1982 for a cri- Lanyon 1992, Harshman 1994). Its limitations tique of Cracraft's classification). are shown by the fact that it does not support Summarising the above, current evidence sister group relationship between Phalacrocor- thus more convincingly supports monophyly acidae and Anhingidae (Sibley & Ahlquist of the taxon (Scopidae + (Balaenicipitidae + 1990, van Tuinen et al. 2001), which share a Steganopodes)) than monophyly of the taxon number of unique derived characters as, for ex- (Phaethontidae + Steganopodes). Accordingly, ample, an ossified ªoccipital styleº at the cau- G. Mayr ´ Shoebill phylogeny 169 dal end of the cranium. Mitochondrial genes more convincingly support assignment of Ba- on the other hand probably evolve too rapidly laeniceps to any of the ªciconiiformº birds, to be useful in the detection of basal divergen- and omitted from his analysis one of the most ces among birds (Groth & Barrowclough characteristic characters shared by Balaenici- 1999). The analysis of Hedges & Sibley pitidae, Scopidae and the Steganopodes, the (1994) was critically evaluated by Farris et al. laterally protruding facies articularis acrocora- (1999), who concluded that the data ªare too coidea of the furcula. Webbing of toes occurs poorly constructed to provide well-supported in many unrelated aquatic birds (see above), resolution of any larger divisions of the in- but it is difficult to explain by convergence the groupº. above-listed derived characters of the pectoral Siegel-Causey (1997) listed a single mor- girdle in birds with such different flight styles phological character that supports monophyly as hamerkops, shoebills and gannets. of a taxon including Pelecanidae, Fregatidae and Balaenicipitidae, i. e. the fusion of the fur- Acknowledgements cula with the apex carinae of the sternum. This I thank CeÂcile Mourer-ChauvireÂ (UniversiteÂ Claude Ber- character in isolation is of questionable phylo- nard, Lyon) for making available to me specimens in the genetic significance since the furcula abuts to osteological collection of her institute, and S. TraÈnkner an articulation facet of the carina sterni in all (Forschungsinstitut Senckenberg) for taking the photo- pelecaniform birds as well as in the Ciconii- graphs. I further thank D. S. Peters and C. Mourer-ChauvireÂ for reviewing the manuscript. dae; fusion could thus easily have occurred several times independently. Cottam (1957) noted that within the Ciconiidae the furcula is References fused to the apex carinae in some specimens of Leptoptilos. Livezey & Zusi (2001) did not Bartlett, A. D. (1861): On the affinities of Balaeni- give the characters supporting their phylogeny ceps. Proc. Zool. Soc. London 1861: 131±134. which also resulted in sister group relationship Baumel, J. J. & Witmer, L. M. (1993): Osteologia. In: Baumel, J. J., King, A. S., Breazile, J. E., of Balaenicipitidae and Pelecanidae, within a Evans, H. E. & Vanden Berge, J. C. (Eds.): Hand- monophyletic taxon Pelecaniformes. However, book of avian anatomy: Nomina Anatomica these authors did not include postcranial char- Avium. Publications of the Nuttall Ornithological acters in their analysis and if there are conver- Club 23: 45±132. gent similarities between the shoebill and peli- Beddard, F. E. (1884): A contribution to the anatomy cans, they are likely to be due to the huge bill of Scopus umbretta. Proc. Zool. Soc. London of these taxa and thus mainly effect the charac- 1884: 543±553. ters studies by these authors, i. e. the skull and Beddard, F. E. (1888): On certain points in the Vis- the vertebral column. ceral Anatomy of Balaeniceps rex bearing on its Affinities. Proc. Zool. Soc. London 1888: Cracraft (1985) considered the derived simi- 284±290. larities between Balaeniceps and pelecaniform Beddard, F. E. (1898): The structure and classifica- birds to be due to ªmechanical responses to tion of birds. London. similarities in feeding behaviourº. However, Bock, W. J. (1960): Secondary articulation of the apart from the fact that, for example, the avian mandible. Auk 77: 19±55. shared derived eggshell structure cannot be ex- BoÈhm, M. (1930): UÈ ber den Bau des jugendlichen plained in this way, most of the above-listed SchaÈdels von Balaeniceps rex nebst Bemerkun- gen uÈber dessen systematische Stellung und uÈber characters are also present in Scopus, which das Gaumenskelett der VoÈgel. Z. Morph. OÈ kol. has very different living and feeding habits Tiere 17: 677±718. from those of Balaeniceps and pelecaniform Cottam, P.A. (1957): The pelecaniform characters birds (del Hoyo et al. 1992). Moreover, Cra- of the skeleton of the Shoebill Stork, Balaeniceps craft (1985) did not mention characters which rex. Bull. Brit. Mus. (Nat. Hist.) Zool. 5: 51±72. 170 Journal fuÈr Ornithologie 144, 2003

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Appendices

Appendix I. Character descriptions. mon ancestor of Phalacrocoracidae and An- hingidae and also coded the character as 1. Upper beak, praemaxilla with sharply present for this taxon. hooked tip (Fig. 3; Cottam 1957): absent (0), present (1). The beak of extant adult 2. External narial openings greatly reduced or Sulidae has a slight terminal hook only, completely absent: no (0), yes (1). which might be connected with the charac- 3. External nostrils tubular: no (0), yes (1). teristic plunge-diving of boobies and gan- This character is unique to the Procellarii- nets. Because a hook is present in hatch- formes. lings of the Sulidae (Cottam 1957), I 4. Upper beak, marked furrow distal of nasal assume its weak development in adult Suli- opening (Fig. 3; ªnasal grooveº of Cottam dae to be derived and accordingly coded 1957): no (0), yes (1). As noted by Beddard the character as present. Likewise, the ab- (1898), this furrow ªis suggestive of a re- sence of this character in the Anhingidae is cently closed, more elongated nostril, like probably due to the unique foraging meth- that of the cranesº (which indeed occurs in od of these birds (spear-fishing); I assume some juvenile pelecaniforms, see Fig. 9 in that the beak was hooked in the last com- Olson 1977). The absence of this character 172 Journal fuÈr Ornithologie 144, 2003

in the Anhingidae is here considered to be 14. Processus paroccipitales protruding in autapomorphic for this taxon and con- caudal direction: no (0), yes (1). nected with its foraging behaviour (see 15. Recessus tympanicus dorsalis: not as fol- above). The furrow in Ardeidae is much lows (0), greatly enlarged and situated ros- wider and shallower than that in the other trally to the articular facets of the quadrate taxa. (1), enlarged and situated laterally to the 5. Skull, ossified septum nasale: absent (0), articular facets of the quadrate (2) (Saiff present (1). 1978). Usually the recessus tympanicus is 6. Conchae nasales greatly reduced or com- small and situated between the articular pletely absent: no (0), yes (1); (after Tech- facets of the quadrate. This character was nau 1936). incorrectly coded as present for the Hydro- 7. Os ectethmoidale: not as follows (0), ves- batidae by Cracraft (1985) (see also Saiff tigial (1), completely reduced (2). The Ar- 1978); it is further absent in some Procel- deidae show a great variation in the size of lariidae (e. g. Bulweria bulwerii). the os ectethmoidale (see Figs. 6±8 in 16. Fossae temporales extending to midline of Payne & Risley 1976); I consider a well- cranium: no (0), yes (1). developed bone primitive for the taxon and 17. Fossae glandulae nasales very marked and accordingly coded it with ª0º (see also Cra- situated on dorsal surface of supraorbital craft 1968 for a survey on the morphology margin of orbitae: no (0), yes (1). of the ectethmoid within extant birds). This 18. Quadratum, condylus medialis: not as fol- character was coded as ordered. lows (0), with marked, rostrally projecting, 8. Ossa maxillaria, processus maxillopalatini concave articular surface (1), with rather greatly enlarged and spongy: no (0), yes indistinct, laterally projecting, concave ar- (1). ticular surface (2). This character was re- 9. Os palatinum, pars choanalis very deep in ferred to as either ªlateral grooveº, ªlateral dorso-ventral direction: no (0), yes (1). concavityº, ªincurved surfaceº, or ªanteri- 10. Ossa palatina fused along their midline or lipº by Bock (1960) who considered it a (Fig. 1 in Cottam 1957): no (0), yes (1). medial brace for protection of the mandi- The ossa palatina appear to be completely ble. fused in the specimens of Fregata I inves- 19. Quadratum, processus orbitalis reduced: tigated (three skulls in the collection of the no (0), yes (1). Forschungsinstitut Senckenberg); Cracraft 20. Columella tubular (Fig. 1 in Feduccia (1985) found them to be only caudally 1977): no (0), yes (1). (ªposteriorlyº) fused. 21. 8th±11th cervical vertebrae: processus 11. Os palatinum an almost completely flat carotici ankylosed along midline, forming horizontal plate: no (0), yes (1). This char- an osseous canal: no (0), yes (1). acter is unique to Sulidae, Anhingidae and 22. Furcula, extremitas omalis with strongly Phalacrocoracidae. developed, laterally protruding facies ar- 12. Vomer: present (0), absent (1). ticularis acrocoracoidea which articulates 13. Well-developed processus basipterygoidei with a distinct ovoid facies articularis that articulate with the ossa pterygoidea: clavicularis of the coracoid (Fig. 4): no present (0), absent (1). In the Hydrobatidae (0), yes (1). The extremitates omales of and Pelecanidae rudimentary processus furcula and coracoid are fused in the Fre- basipterygoidei are present which do not, gatidae, but according to Cottam (1957), however, articulate with the ossa pterygoi- the presence of this character can be ªin- dea. ferred from the suturesº in juvenile speci- G. Mayr ´ Shoebill phylogeny 173

mens; Olson (1977), however, found it ab- 36. Tibiotarsus, proximal end, cristae cne- sent in Eocene stem group representatives miales strongly proximally protruding: no of the Fregatidae and I have coded it as un- (0), yes (1). known. 37. Tibiotarsus, distal end bent medially, con- 23. Furcula: apophysis furculae: not as fol- dylus medialis protruding farther distally lows (0), abutting with an articular facet at than condylus lateralis: no (0), yes (1). the apex carinae of the carina sterni (1), 38. Tarsometatarsus, hypotarsus with tendon fused with the apex carinae of the carina of musculus flexor digitorum longus and sterni (2). This character was coded as or- m. flexor hallucis longus enclosed in bony dered. canal (Fig. 6): no (0), yes (1). 24. Coracoid, foramen nervi supracoracoidei: 39. Tarsometatarsus, hypotarsus without cris- absent (0), present (1). Within the Ciconii- tae intermediae, crista lateralis separated dae, a foramen nervi supracoracoidei oc- from crista medialis by a deep sulcus: no curs in Leptoptilos. (0), yes (1). 25. Coracoid, tip of processus procoracoideus 40. Tarsometatarsus, hypotarsus with crista bent towards extremitas omalis: no (0); medialis strongly protruding: no (0), yes yes (1). (1). 41. Musculus expansor secundariorum vestig- 26. Coracoid, extremitas sternalis, processus ial or completely absent: no (0), yes (1); lateralis greatly elongated: no (0), yes (1). (after Forbes 1882, Beddard 1898, Mitch- 27. Sternum, caudal portion of carina sterni re- ell 1913). duced, apex carinae strongly cranially pro- 42. Musculus ambiens: present (0), extremely truding: no (0), yes (1). vestigial or absent (1); (after Beddard 28. Sternum, dorsal surface with numerous 1884, Vanden Berge 1970, McKitrick pneumatic foramina along midline and lat- 1991). eral margins (Fig. 5): no (0), yes (1). 43. Musculus gastrocnemius, fourth head: ab- 29. Sternum, distal margin, trabecula mediana sent (0), present (1); (after Beddard 1884, very short, reaching much less far distally Vanden Berge 1970, McKitrick 1991). than trabeculae laterales: no (0), yes (1). 44. Musculus flexor cruris lateralis, pars ac- 30. Humerus, shaft straight: no (0), yes (1). cessoria (ªYº muscle in the formula in Usually the shaft of this bone is more or Tab. IX.1 of George & Berger 1966): less sigmoidally bowed. present (0), absent (1); (after McKitrick 31. Humerus, proximal end, sulcus transversus 1991). very deep, long and rectangular-shaped: 45. Musculus caudofemoralis, pars pelvica no (0), yes (1). (ªBº muscle in the formula Tab. IX.1 of George & Berger 1966): present (0), ab- 32. Humerus, crista deltopectoralis strongly sent (1); (after Beddard 1884, McKitrick protruding and triangular: no (0), yes (1). 1991). 33. Humerus, crista deltopectoralis strongly 46. Powder down patches on back of rump: reduced: no (0), yes (1). absent (0), present (1); (after Beddard 34. Humerus, large and strongly protruding 1898, Mitchell 1913). The presence of processus supracondylaris dorsalis present: powder down patches was one of the no (0), yes (1). major reasons for considering Balaeniceps 35. Phalanx proximalis digiti majoris with related to the Ardeidae (Bartlett 1861). well-developed processus internus indicis However, there are only two powder down (terminology after Stegmann 1963): no patches in the former but four to eight in (0), yes (1). herons (Mitchell 1913). 174 Journal fuÈr Ornithologie 144, 2003

47. Gular pouch: absent (0), very inconspicu- 52. Eggs incubated beneath feet: no (0), yes ous and feathered (1), large and naked (2). (1); (Cracraft 1985). This character was in- The homology of the gular pouch of pele- correctly coded by Siegel-Causey (1997) caniform birds is uncertain (Sibley & Ahl- who assumed it to be present in Fregatidae quist 1990, Siegel-Causey 1997). and Balaenicipitidae (Elliot 1992, Orta 48. Three anterior toes: not as follows (0), on- 1992). ly proximal part webbed (1), webbed over 53. Claw of third toe distinctly pectinate on its their entire length (2). In many Ardeidae a medial side: no (0), yes (1). Although short web is present between the fourth some authors considered the claw of the and the third toe, but absent between the third toe of Balaeniceps to be incipiently third and second toe; Balaeniceps lacks pectinate (Giebel 1873, Mitchell 1913), I any webs between the toes. could not find any traces of pectination in 49. Hallux greatly reduced and consisting of the specimens available to me (three skins a single phalanx only: no (0), yes (1). in the collection of the Forschungsinstitut Usually the hallux has to phalanges. Senckenberg). 50. Hallux included in webbed foot (Fig. 7): no (0), yes (1). This character is generally 54. Eggshell covered with layer of microglob- considered to be a synapomorphy of the ular material (amorphous form of calcium Pelecaniformes. carbonate): no (0), yes (1) (Mikhailov 51. Young at hatching: downy (0), naked (1). 1995).

Appendix II. Character matrix of 54 morphological characters for the 14 taxa included in this study (see Appendix I for character definitions). Unknown character states are indicated by ª?º. Tinamidae were used for outgroup comparison.

characters 1234567891011121314151617181920 Tinamidae 00000000000000000000 Ardeidae 000100000000100001200 Ciconiidae 000000121100010000101 Threskiornithidae 00010000100010000100 Diomedeidae 10110000100010101100 Hydrobatidae 10110000000010001100 Procellariidae 101100000000000111100 Scopidae 10011011110010000100 Balaenicipitidae 11011021110010000201 Phaethontidae 0000000000001010000? Fregatidae 11011110010010100000 Pelecanidae 1101112111011020000? Phalacroc./Anhingidae 1101110000111111210210 Sulidae 11011120011111110210 G. Mayr ´ Shoebill phylogeny 175

characters 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 Tinamidae 00000000000000000000 Ardeidae 10001000001000000001 Ciconiidae 001011001001000100010 Threskiornithidae 01 0011000001000100010 Diomedeidae 00010111110101110000 Hydrobatidae 00010100010001110000 Procellariidae 0001010010101011100100 Scopidae 01000001001100100100 Balaenicipitidae 11211001101010100101 Phaethontidae 00110000011100100000 Fregatidae 0 ? 200001111100100000 Pelecanidae 11211011000010101101 Phalacroc./Anhingidae 0110001010101001010101 Sulidae 11101011100010101101

characters 41 42 43 44 45 46 47 48 49 50 51 52 53 54 Tinamidae 0 0 0 0 0 01 0 0 0 0 0 0 0 0 Ardeidae 0 1 0 0 1 1 0 0 0 0 1 0 1 01 Ciconiidae 0 01 1 0 1 0 0 1 0 0 01 0 0 0 Threskiornithidae 0 0 1 0 0 0 0 1 0 0 01 0 0 0 Diomedeidae 1 0 0 1 0 0 0 2 1 0 0 0 0 0 Hydrobatidae 0 0 0 01 0 0 0 2 1 0 0 0 0 0 Procellariidae 1 0 0 1 0 0 0 2 1 0 0 0 0 0 Scopidae 1 1 1 0 1 0 0 1 0 0 0 0 1 1 Balaenicipitidae 1 1 0 0 1 1 0 0 0 0 0 0 0 1 Phaethontidae 1 ? ? 0 1 0 1 2 0 1 0 0 0 0 Fregatidae 1 0 0 1 1 0 2 1 0 1 1 0 1 1 Pelecanidae 1 1 ? 1 1 0 2 2 0 1 1 1 0 1 Phalacroc./Anhingidae 1 0 0 1 1 0 2 2 0 1 1 1 1 1 Sulidae 10011022011111