Ibis (2013), 155, 544–560

Interrelationships of the Threskiornithidae and thephylogenetic position of the Miocene ibis ‘Plegadis’ rand-le-Puy area in central
paganus from the Saint-Ge
FranceVANESA L. DE PIETRI*
Natural History Museum Basel, Basel, Switzerland

The fossil ibis Plegadis paganus is known from the Early Miocene of the Saint-Gerandle-Puy area, France. It was ﬁrst described in the 19th century by Milne-Edwards(1867–1868), who noticed similarities with members of the extant genera Eudocimus
and Plegadis, a view endorsed by subsequent descriptions. The fossil’s present placement within the genus Plegadis is not supported by synapomorphic features, and important differences with members of this genus have been noted in the past. The present
analysis demonstrates that retention of P. paganus in the extant genus Plegadis is nolonger justiﬁed, and it is therefore referred to the new genus Gerandibis. A phylogenetic analysis of 55 osteological characters supports placement of Gerandibis pagana ina clade together with Neotropical taxa. This analysis also allowed for an evaluation of
the relationships among extant threskiornithids. Contrary to results obtained in molecular-based phylogenies, the present analysis supports a basal divergence of crown group
Threskiornithidae into a clade comprising Threskiornis and Platalea and a clade comprising all other ibises. Within the latter, two clades, one made up of Old World taxa andthe other consisting predominantly of New World taxa, were recovered.
Keywords: Early Miocene, fossil birds, Gerandibis pagana, ibis phylogeny.

The Threskiornithidae (ibises and spoonbills) are afamily of wading and terrestrial birds that arefound on all continents except Antarctica, withthe highest species diversity occurring in thetropics and subtropics. Thirteen genera and 32
species are recognized (Matheu & del Hoyo 1992).
Based on the morphology of the bill, the Threskiornithidae have traditionally been subdivided into
two subfamilies, the Threskiornithinae (ibises) and
the Plataleinae (spoonbills). This view has beenchallenged by molecular phylogenetic studies
which, in agreement with results obtained from
DNA–DNA hybridization data (Sibley & Ahlquist
1990), have found the Threskiornithinae to beparaphyletic, with spoonbills recovered as
nested within the other ibis genera (Chesser et al.
2010). Thus, a subdivision of the family intoThreskiornithinae and Plataleinae appears not to*Email: vanesa.depietri@bs.ch© 2013 British Ornithologists’ Union

be warranted, and a deep divergence within extant
Threskiornithidae between New World (e.g.
Eudocimus, Theristicus) and Old World (e.g.
Geronticus, Threskiornis, Platalea) genera has beensuggested (Sibley & Ahlquist 1990, Chesser et al.
2010). To date, few cladistic studies have focusedon the systematic relationships within the Threskiornithidae.
The Palaeogene fossil record of the Threskiornithidae has been discussed in detail by Mayr
(2009). The earliest known representatives of thefamily are members of the genus Rhynchaeites,
stem threskiornithids with a record dating to the
Early and Middle Eocene of Denmark andGermany, respectively (Peters 1983, Mayr 2002a,
Mayr & Bertelli 2011). Further Palaeogene specimens referred to this family include a humerus
from the Late Eocene of England assigned to
Actiornis anglicus Lydekker 1891 (Harrison andWalker 1976, Mayr 2009), a small tibiotarsus from

Early Miocene ibis and phylogeny of Threskiornithidae

the late Middle Eocene of Myanmar (Stidham
et al. 2005), and a tibiotarsus and ulna from theLate Eocene of China (Hou 1982). For most ofthese specimens, an unambiguous referral to theThreskiornithidae has not been possible (Stidham
et al. 2005, Mayr 2009). A reported stem ibis
from the Early Eocene of the Green River Formation, Wyoming, was recently described by Smithet al. (2013), and represents the earliest record of
a putative ibis from North America. The mostcomplete (albeit badly preserved) skeleton of athreskiornithid from the Early Oligocene of Cereste, France, was described by Roux (2002).
The Miocene fossil record of threskiornithids in
Europe is restricted to two species (Mlıkovsky2002), ‘Ibis’ pagana (Milne-Edwards 1868) fromthe Early Miocene of the Saint-Gerand-le-Puy
area, and Geronticus perplexus (Milne-Edwards
1871), from the Middle Miocene of Sansan,
France. The latter fossil was ﬁrst described byMilne-Edwards (1869–1871) as Ardea perplexa,
based on a distal fragment of a humerus. It waslater recognized as an ibis (Cheneval 2000) andplaced in the extant genus Geronticus, although ajustiﬁed genus-level referral may not be possible
from the available material. Fragmentary remainsof ibises have also been reported from the Middle
Miocene of Africa (Dyke & Walker 2008).
The Early Miocene (c. 23–20.5 Ma) ibis I.
pagana from the Saint-Gerand-le-Puy area wasﬁrst described by Milne-Edwards (1867–1868) on
the basis of several postcranial elements and a partial skull. As noted by Olson (1981), the genericname Ibis Lacepede 1799, used to refer to somespecies of storks of the genus Mycteria (Ciconiidae), led Brodkorb (1963) to list I. pagana as Eudocimus paganus in his Catalogue of Fossil Birds, agenus under which it had already been listed by
Sharpe (1899). Olson (1981) recognized postcranial similarities between I. pagana and the extant
genus Plegadis, albeit only based on a distal tarsometatarsus, and thus referred the fossil ibis to thisgenus. The most recent comprehensive revision of
the Plegadis paganus fossil material was undertaken
by Cheneval (1984) who, despite noticing several
osteological differences from members of thegenus Plegadis, retained Olson’s generic nomenclature. Harrison (1986) suggested that based on
humeral characters, P. paganus should be referredto the Eocene genus Actiornis (Harrison andWalker 1976), but this referral was not formallyestablished.

545

This paper represents the ﬁrst osteological phylogeny aimed at clarifying the relationships within
the Threskiornithidae. The analysis was primarily
conceived to determine how the Early Miocene
ibis P. paganus relates to extant ibises, and toassess what biogeographical implications result
from the obtained phylogeny. Additionally, a taxonomic review and a brief description of skeletal
elements of P. paganus in comparison with a representative sample of extant threskiornithids arepresented.
METHODS
Anatomical terminology follows Baumel and Witmer (1993). The fossil specimens described herein
are deposited at the Department des Sciences dela Terre, Universite Claude Bernard, Lyon I,
Villeurbanne, France (FSL), Museum Nationald’Histoire Naturelle, Paris, France (MNHN), andNaturhistorisches Museum Basel, Switzerland(NMB). This assessment is based primarily on thefossil material housed in NMB, with the exception of the previously unknown, almost complete
skull from MNHN (MNHN SG. 10043). The
postcranial skeleton of P. paganus has been comprehensively described by Milne-Edwards (1867–
1871) and Cheneval (1984). For this reason, I
focus on previously unrecognized features and on
several of the characters used in the phylogenetic
analysis.
Comparisons were made with skeletons of thefollowing extant taxa in the collections of NMB
and Forschungsinstitut Senckenberg Frankfurt am
Main, Germany (SMF). Numbers in parentheses
indicate the number of individuals examined:
Olive Ibis Bostrychia olivacea (1, skull), Hadada
Ibis Bostrychia hagedash (1), Scarlet Ibis Eudocimus
ruber (3), Southern Bald Ibis Geronticus calvus (1,skull), Northern Bald Ibis Geronticus eremita (2),Madagascar Ibis Lophotibis cristata (1), African
Spoonbill Platalea alba (1, skull), Roseate Spoonbill Platalea ajaja (1), Eurasian Spoonbill Platalea
leucorodia (4), White-faced Ibis Plegadis chihi (1,skull), Glossy Ibis Plegadis falcinellus (4), Puna Ibis
Plegadis ridgwayi (1), Red-naped Ibis Pseudibis papillosa (1), Black-faced Ibis Theristicus melanopis (2),African Sacred Ibis Threskiornis aethiopicus (2).
Comparisons were also made with the following
taxa: Ciconiidae: White Stork Ciconia ciconia;
Ardeidae: Grey Heron Ardea cinerea, Purple
Heron Ardea purpurea.

© 2013 British Ornithologists’ Union

546

V. L. De Pietri

Although only skulls were available for some ofthese taxa (and were therefore not included in thecladistic analysis), these do not differ in the mentioned characters from other members of theirrespective genera.
Phylogenetic analysis
The main aim of this study was to determine thephylogenetic afﬁnities of P. paganus, and for thispurpose only characters that could be deﬁned forthe fossil ibis were scored in extant taxa. Thus, 55
characters were coded for 12 terminal taxa within
the Threskiornithidae (mentioned above), representing nine of the 13 extant genera (Appendices 1 and 2). C. ciconia and A. cinerea werechosen as outgroups. The works of Ferreira andDonatelli (2005), Livezey and Zusi (2006, 2007),
Scoﬁeld et al. (2010), Smith (2010), and Worthy
et al. (in press) were consulted for additional characters. All characters were treated as unordered.
Phylogenetic analyses were performed with theheuristic search modus of NONA 2.0 (Goloboff1993) through the Winclada 1.00.08 interface(Nixon 2002), using the following commands: hold10000, hold/10, mult*1000 and max*. Bootstrap
values were calculated under the following settings:
1000 replicates, with three searches holding one
tree per replicate, and tree bisection-reconnection(TBR) branch swapping without max*.

interorbital region of frontal, (2) relatively large
fonticuli occipitales, (3) short rostrocaudal fusionof ossa palatina in ventral view, (4) small fonticuli
orbitocraniales, (5) prominent tuberculum ancorae
ligamentosa on margo medialis of extremitas sternalis of coracoid, (6) dorsal facet of crista articularis sternalis of coracoid overhanging ventral facet,(7) fossa m. brachialis of humerus moderately
deep, (8) marked tubercle on crista lateralis sulci
patellaris of femur, (9) poorly developed epicondylus medialis of tibiotarsus, (10) trochlea metatarsi
IV of tarsometatarsus extending distally past trochlea metatarsi II, (11) crista medialis hypotarsi projecting plantarly beyond crista lateralis hypotarsi,(12) prominent crista lateralis hypotarsi separated
from cristae hypotarsi intermediae by well-marked
sulcus for musculus ﬂexor hallucis longus and (13)conspicuous dorsal opening of canalis interosseus
distalis.
Of the above mentioned characters, (1), (2),(3), (4), (6), (7) and (9) are shared with E. ruber
and species of Plegadis and (3), (6) and (7) are
additionally present in T. melanopis. Features (11)and (12) distinguish this taxon from E. ruber andspecies of Plegadis. Gerandibis agrees with speciesof Plegadis and B. hagedash in character (13) andwith B. hagedash, G. eremita and P. papillosa incharacter (5). Character (8) is autapomorphic for
the fossil genus.
Gerandibis pagana (Milne-Edwards 1867–1871)

RESULTS
Systematic palaeontology
Threskiornithidae Richmond 1917.
Gerandibis gen. nov
Type species

Gerandibis pagana (Milne-Edwards 1868); typespecies by monotypy.

Figure 1a, e, j, m; Fig. 2a, d, f–j, k, n–o, r.
Ibis pagana Milne-Edwards 1868: 450, pl. 69,
ﬁgs 2–8; pl. 57, ﬁgs 12–90; pl. 71, ﬁgs 1–12.
Milnea gracilis Lydekker 1891: p. 72.
Eudocimus paganus (Milne-Edwards 1868):
Brodkorb 1963: p. 278.
Plegadis paganus (Milne-Edwards 1868): Olson
1981: pp. 165–166, ﬁg. 1.
Lectotype

Derivation of name

MNHN 8693 (right tarsometatarsus), chosen by
Cheneval (1984).

From Saint-Gerand-le-Puy, genus name is feminine.

Diagnosis

Same as for genus; see also Cheneval (1984).

Diagnosis

Gerandibis gen. nov. is a monotypic genus for thesmall ibis from the Saint-Gerand-le-Puy area, characterized by a combination of the following features (see also Cheneval 1984): (1) notched© 2013 British Ornithologists’ Union

Locality and age

Saint-Gerand-le-Puy area, Early Miocene, Aquitanian, MN1–MN2 (c. 23–20.5 Ma), but see De
Pietri et al. (2011a,b).

Early Miocene ibis and phylogeny of Threskiornithidae

547

Newly referred specimens

Remarks(L, left; R, right): MNHN SG 10043 (complete
cranium with caudal portion of maxilla); NMB
S.G.15819, NMB S.G.20538 (R scapulae missing
caudal end), NMB Au.94, NMB S.G.12684 (Lscapulae missing caudal end), FSL 8331272 (Rcoracoid), NMB M.A.618 (R coracoid), NMB
M.A.627 (L coracoid), NMB M.A.671 (Rcoracoid), NMB M.A.1090 (R coracoid), NMB
M.A.1412 (R coracoid), NMB S.G.1217 (Rcoracoid), NMB S.G.17722 (R coracoid), NMB
S.G.19327 (R coracoid), NMB S.G.21628 (L coracoid), NMB S.G.21889 (L coracoid), NMB
S.G.6233 (partial L coracoid), NMB S.G.6236(partial R coracoid), NMB S.G.7462 (R coracoid),
NMB S.G.7727 (R coracoid), NMB Au.29 (distal
R humerus), NMB M.A.1571 (L humerus), NMB
M.A.1574 (proximal L humerus), NMB M.A.1587(distal L humerus), NMB Ph.2765 (L humerus),
NMB Sau.2064 (distal L humerus), NMB
S.G.6622 (L humerus), NMB S.G.6623 (distal L
humerus), NMB S.G.6228 (proximal L humerus),
NMB S.G.20625 (distal L humerus), NMB
S.G.21926 (R humerus), NMB S.G.21948 (proximal R humerus), NMB M.A.1596 (L ulna), NMB
M.A.2531 (L ulna), NMB Ph.3516 (L ulna), NMB
S.G.4018 (R ulna), NMB S.G.6221 (proximal Rulna), NMB S.G.7247 (L ulna), NMB S.G.17304(L ulna), NMB S.G.19340 (L ulna), NMB
Au.1488 (distal L carpometacarpus), NMB Chr.
421 (L carpometacarpus), NMB S.G.23395 (Rcarpometacarpus), NMB S.G.12019 (R femur),NMB S.G.17461 (L femur), NMB S.G.17196 (Lfemur), NMB Au.173 (R tibiotarsus), NMB
S.G.4016 (R tibiotarsus), NMB S.G.6698 (L tibiotarsus), NMB M.A.1688 (R tibiotarsus), NMB
S.G.6222 (distal R tibiotarsus), NMB Au.35 (proximal L tarsometatarsus), NMB Au.84 (proximal R
tarsometatarsus), FSL 442811 (R tarsometatarsus),
FSL 442813 (R tarsometatarsus), NMB Chr. 694(distal L tarsometatarsus), NMB S.G.7397 (Rtarsometatarsus), NMB S.G.17770 (L tarsometatarsus), NMB S.G.7732 (juvenile, R tarsometatarsus), NMB S.G.7395 (juvenile, L tarsometatarsus),NMB S.G.19380 (L tarsometatarsus).

The type material of G. pagana was listed byCheneval (1984) and Mlıkovsky (2002) underP. paganus. Tibiotarsi NMB S.G.4016 and NMB
S.G.6698 were incorrectly referred to the Early
Miocene scolopacid bird Elorius limosoides by De
Pietri and Mayr (2012), and should therefore not
be considered in any future discussion regarding
this taxon.

Measurements

Measurements for G. pagana were provided byMilne-Edwards (I. pagana, 1867–1868, p. 459)
and Cheneval (P. paganus, 1984, p. 83). For size
comparisons with some extant threskiornithids, see
Table 1.

Description and comparisons

The overall appearance of the skull (Fig. 1a) is
most similar to that of E. ruber (Fig. 1b). As in all
threskiornithids, the interorbital region of the os
frontale is wide (Fig. 1a–d), but contrary to thecondition observed in most ibises (e.g. P. papillosa,Fig. 2d), the orbital rims are strongly notched in
Gerandibis, Eudocimus and species of Plegadis(Fig. 1a–c). The lateral rim of the interorbital andsupraorbital portions of the os frontale (Fig. 1a)are wide in G. pagana and E. ruber, whereas they
are dorsoventrally compressed in species of Plegadis and most other ibises. The fonticuli orbitocraniales (Fig. 1j) are large but, unlike members ofArdeidae, the orbital foramen does not occupy
most of the interorbital septum.
Only the caudal portion of the beak is preserved in MNHN SG 10043. As in E. ruber, there
is a depression where the frontal meets the os nasale, a condition also absent in species of Plegadis.
Contrary to the condition present in other ibises
such as Geronticus and Pseudibis, the fossae temporales are moderately deep, reaching towards the
midline of the cranium (Fig. 1e). The processus
postorbitales (Fig. 1e) are proportionally longer
than in E. ruber and species of Plegadis (Fig. 1f,g).
Unlike in these taxa, the processus paraoccipitales(Fig. 1j) are relatively short, resembling the condition in most other ibises (e.g. T. melanopis, P. papillosa).
In the occipital region, the prominentia cerebellaris does not bulge caudally as prominently as inmembers of Plegadis (Fig. 1c). The fonticuli occipitales are relatively large (Fig. 1e). There are wellmarked depressions dorsal to the crista nuchalistransversa as in E. ruber. The paired sulci venarum
occipitalis externae, lateral to the foramen magnum, are wide and deep as in most threskiornithids, most closely resembling those of E. ruber.
The maxillopalatine complex (Fig. 1j) is similar
to that of species of Plegadis and, contrary to thecondition observed in several threskiornithids© 2013 British Ornithologists’ Union

548

V. L. De Pietri

Table 1. Selected measurements for Gerandibis pagana (Milne-Edwards 1868) in comparison with some extant threskiornithids. For
the extant taxa, measurements of the left and right skeletal elements were averaged. Measurements of G. pagana are after Cheneval(1984). All measurements are in millimetres and were rounded off to the nearest tenth.

Measurement
Coracoid
Length
Humerus
LengthProximal width
Distal width
Shaft width
Ulna
LengthProximal width
Distal width
Shaft width
Femur
LengthProximal width
Distal width
Tibiotarsus
LengthProximal width
Distal width
Shaft width
Tarsometatarsus
LengthProximal width
Distal width
Shaft width

Gerandibis
paganaPseudibis
papillosa

Plegadis
falcinellus

Eudocimus
ruber

Theristicus
melanopis

36.1 (32.9–39)

52.5

42.2

42.7

51.4

77.8 (73.0–83.0)
19.4 (17.8–20.8)
12.5 (11.3–13.3)
5.6 (4.3–6.2)

120.5
26.3
20.5
9.2

97.5
20.2
14.2
6.5

90.3
21.3
15.3
6.3

117.1
27.6
21
9.4

87.2 (79.0–92.6)
8.0 (7.0–8.8)
5.7 (5–7.4)
3.8 (3.1–5.1)

134.1
13.7
11.4
6.4

110
9.9
9.3
4.8

103
9.4
8.4
4.3

129.3
13.7
12.3
7

47.1 (44.6–51.2)
8.9 (8.0–9.9)
8.9 (8.2–10.3)

62.5
13.8
14.2

60
11.4
10.7

59.3
11.5
12.2

66.2
15.4
15.5

91.0 (85.7–97.6)
7.2 (6.5–8.0)
7.1 (6.3–8.0)
3.7 (3.9–4.1)

114.7
11.8
11
5.7

137.5
9.4
9
4.9

117.7
10.9
9.6
4.8

126.9
12.5
12.4
6.5

62.7 (56.2–69.3)
8.3 (7.7–9.1)
7.1 (7.7–9.2)
3.5 (3.3–8.4)

74.8
13.1
12.9
5.3

103.8
9.8
9.7
4

83.6
11.1
11.6
4.4

86.7
14.1
14
5.6

(e.g. Geronticus, Pseudibis, Lophotibis), the processus maxillopalatinus is not fused with the os palatinum (Fig. 1l). Also, the palatine bears aconspicuous concavitas palatis, which is pierced asin several threskiornithids (Fig. 1m); this condition
is absent in species of Plegadis (Fig. 1n). In ventral
view, the ossa palatina are fused in the midline
and, unlike in several threskiornithids (e.g. Pseudibis, Geronticus, Bostrychia), this fusion is rostrocaudally short (Fig. 1m–o).
The coracoid of G. pagana (Fig. 2a) closely
resembles the corresponding bone of extant
members of Plegadis, Eudocimus and Theristicus.
As in all threskiornithids, a foramen nervi supracoracoidei is present. In dorsal view, the shaft ofthe coracoid of G. pagana bears a well-deﬁned
scar that traverses the shaft diagonally in a mediolateral direction, delimiting the omal outline of
the impressio m. sternocoracoidei (Fig. 2a). In
some ibises (e.g. Bostrychia, Lophotibis) this scar
is situated at mid-shaft, which is also the case in
Gerandibis; by contrast, it is situated closer to© 2013 British Ornithologists’ Union

the sternal end of the coracoid in Geronticus andPseudibis (Fig. 2c). The impressio m. sternocoracoidei is somewhat shallow. At the sternal end,
the dorsal facet of the crista articularis sternalis
overhangs the ventral facet, a condition that is
also present in E. ruber, species of Plegadis andT. melanopis (Fig. 2b). In all other examinedthreskiornithids, the ventral facet of the crista
articularis sternalis extends further sternally thanthe dorsal facet (Fig. 2c). Tuberculum ancorae
ligamentosa (sensu Livezey & Zusi 2006) is welldeveloped and angular in G. pagana (Fig. 2a); assuch, it is also present in several other ibises
such as Bostrychia, Pseudibis and Geronticus(Fig. 2c).
The scapula of G. pagana (Fig. 2d) does notdiffer markedly from the corresponding bone ofother threskiornithids. There is a relatively deep
depression on the medial side of the acromion, as
in Eudocimus and species of Plegadis, which isabsent in members of Platalea (Fig. 2e) and
T. aethiopicus.

Early Miocene ibis and phylogeny of Threskiornithidae

(a)

(b)

(c)

(d)

(e)

(j)

(f)

(g)

(h)

(i)

(m)

(p)

(k)

549

(q)

(n)
(r)

(l)

(o)

(s)

 rand-le-Puy area, France, in
Figure 1. Skull of Gerandibis pagana (Milne-Edwards 1868) from the Early Miocene of the Saint-Ge
comparison with cranial elements of extant Threskiornithidae. G. pagana (MNHN SG 10043) skull in dorsal (a), occipital (e), lateral(j) and lateroventral (m) views. Skull of Eudocimus ruber in dorsal (b) and occipital (F) views. Skull of Plegadis chihi in dorsal (c),occipital (g), lateral (k) and ventral (n) views, rostrum maxillare in ventral view (q), and lateral view of right ramus mandibulae (r).
Pseudibis papillosa skull in dorsal (d), occipital (h) and ventral (o) views, rostrum maxillare in ventral view (p), and lateral view of rightramus mandibulae (s). (i) Skull of Platalea leucorodia in occipital view. (l) Skull of Geronticus eremita in lateral view. cf, caudal fenestrae; cp, concavitas palati; fo, fonticuli occipitales; foc, fonticulus orbitocranialis; fop, fusion of ossa palatina; ft, fossa temporalis; iof,
interorbital area of os frontale; lrof, lateral rim of the interorbital and supraorbital portions of the os frontale; op, os palatinum; or,orbital rim of frontal; pc, prominentia cerebellaris; pmp, processus maxillopalatinus; poc, processus paraoccipitales; ppo, processus
postorbitales; pps, processus parasphenoidales. (e–i) and (p–q) are not to scale. Scale bars: 10 mm.

© 2013 British Ornithologists’ Union

550

V. L. De Pietri

The proximal end of the humerus shows little
variation within Threskiornithidae; the pneumaticforamen is relatively small as in most threskiornithids (Fig. 2g), although there are some exceptions(e.g. G. eremita). The distal end is a very close
match to that of E. ruber, bearing a deeper fossa
m. brachialis (Fig. 2f) compared with that of someother ibises (e.g. Plegadis).
As with the humerus, the overall appearance of
the ulna (Fig. 2h) does not seem to vary muchwithin threskiornithids. Unlike in T. aethiopicus andspecies of Platalea, a noticeable, albeit shallow,
round depressio radialis, proximal to the sulcus
intercondylaris, is present. The carpometacarpus ofmembers of Threskiornithidae differs primarily inproportions among taxa. Unlike the carpometacarpus of Gerandibis, the corresponding bone of species of Plegadis is very long and slender; inGerandibis and most other threskiornithids the os
metacarpale majus is proportionally short.
The femur of Gerandibis (Fig 2i–j) is similar tothat of other ibises. There is, however, awell-marked tubercle on the crista lateralis sulci
patellaris, proximal to the sulcus patellaris, whichis also present in A. cinerea. As in all other ibises,
the tuberculum m. gastrocnemialis is well developed.
The proportions of the tibiotarsus and tarsometatarsus of G. pagana closely resemble thoseobserved in E. ruber and T. melanopis, with thetarsometatarsus being about two-thirds the lengthof the tibiotarsus. These elements are more slenderin Gerandibis. Although leg elements are also very
long and slender in species of Plegadis (Fig. 2m,p), the ratio of the tarsometatarsus to tibiotarsus ismuch higher. As observed by Roux (2002), a proportionally much shorter tarsometatarsus is present
in Geronticus, Pseudibis, Lophotibis and Bostrychia,
a condition that may well have been plesiomorphic for Threskiornithidae, as evidenced in thestem ibis Rhynchaeites (e.g. Mayr 2002a, 2009,
Mayr & Bertelli 2011). A record of a putative stem
ibis from the Early Eocene of the Green River formation suggests that proportionally longer limb
elements than in Rhynchaeites may have been present in the specimen (Smith et al. 2013). Within
Threskiornithidae, a proportionally short tarsometatarsus is also present in some New World taxa
not available for this study, such as in the Green
Ibis Mesembrinibis cayennensis and in the Barefaced Ibis Phimosus infuscatus (Miller & Bowman
1956).

© 2013 British Ornithologists’ Union

As already indicated, tibiotarsi NMB S.G.4016
and NMB S.G.698 were erroneously attributed tothe scolopacid bird E. limosoides from the Early
Miocene of Saint-Gerand-le-Puy by De Pietri andMayr (2012). Although superﬁcially similar to thecorresponding bone of the Black-tailed Godwit Limosa limosa, contrary to the condition in mostcharadriiforms, the medial and lateral condyles
are approximately the same size. Additionally, a
relatively well-marked intercondylar prominence
is usually present in Threskiornithidae (Fig. 2m)
but is absent in the scolopacid L. limosa. Thisfeature was not visible in the tibiotarsi describedby De Pietri and Mayr (2012), but the examination of further material has corroborated thatthese tibiotarsi can only be attributed to G. pagana. As in extant Threskiornithidae, the sulcus
extensorius is situated medially (Fig. 2k). Gerandibis further resembles several other ibises in theabsence of a well-marked epicondylus medialis, acondition present in P. papillosa and G. eremita(Fig. 2l).
The proportions of the tarsometatarsus ofG. pagana (Fig. 2n–o), with a proportionally longshaft, are similar to those of most threskiornithids,
although it is not as slender as the tarsometatarsusof species of Plegadis. In other ibises such as Pseudibis and Geronticus, the tarsometatarsus is proportionally short and stout (Fig. 2q).
The overall morphology of the hypotarsus of
Gerandibis (Fig. 2r) is similar to that of otheribises (except Platalea and Threskiornis, in which
there is a single wide and fully open sulcus hypotarsi). Contrary to the condition in Plegadis andEudocimus, the crista medialis hypotarsi protrudes
farther plantarly than the crista lateralis hypotarsi(Fig. 2r–v). This feature was also noticed by Cheneval (1984), and this conﬁguration is also found in
Threskiornis, Geronticus, Theristicus and Pseudibis,
among other taxa. The crista lateralis hypotarsi
does not extend plantarly past the cristae hypotarsi
intermediae and, as in most threskiornithids, thesulcus for musculus ﬂexor hallucis longus is apparent (Fig. 2u). Contrary to this condition, the hypotarsus of Eudocimus and species of Plegadis ismuch narrower than in all other ibises, and thecrista lateralis hypotarsi has been greatly reduced,
resulting in a very shallow sulcus for musculus
ﬂexor hallucis longus (Fig. 2s, u). As in all Threskiornithidae, there is a well-marked tubercle lateral
to the cotyla lateralis (Fig. 2t), and the tuberculum
m. ﬁbularis brevis is well developed.

Early Miocene ibis and phylogeny of Threskiornithidae

(a)

(b)

551

(c)

(d)

(f)

(g)
(h)

(e)

(i)

(j)

(k’)

(n)

(r)
(k)

(l)

(o)

(s)

(p)

(t)

(u)

(q)

(v)

(m)

At the distal end, there is a conspicuous dorsal
opening of canalis interosseus distalis (intertrochlear foramen), distal to the foramen vasculare
distale (Fig. 2n), which had already been reported
by Olson (1981) and Cheneval (1984). Thiscondition appears to be variable within specimensof G. pagana, as it was not apparent in all

specimens. Contrary to what was reported by Olson (1981), the presence of a conspicuous dorsal
opening of canalis interosseus distalis is not, within
Threskiornithidae, only present in the extant genus
Plegadis (Fig. 2p), but a similar conﬁguration tothat of P. ridgwayi was found in the examined
specimen of B. hagedash, and in some individuals© 2013 British Ornithologists’ Union

552

V. L. De Pietri

rand-le-Puy area,
Figure 2. Postcranial bones of Gerandibis pagana (Milne-Edwards 1868) from the Early Miocene of the Saint-Ge
France, in comparison with skeletal elements of some extant Threskiornithidae. G. pagana: right coracoid (FSL 8331272) in dorsal
view (a), right scapula (NMB S.G.15819) in ventral view (d), left humerus (NMN M.A.1571) in cranial (f) and caudal (g) views, left
ulna (NMB Ph.3516) in ventral view, left femur (NMB S.G.17196) in caudal (i) and cranial (j) views, right tibiotarsus (NMB S.G.4016)
in cranial view (k, distal end enlarged in k’), right tarsometatarsus (FSL 442813) in dorsal (n) and plantar (o) views, right tarsometatarsus (FSL 442811) in proximal view (r). Theristicus melanopis: left coracoid in dorsal view (b), proximal view of right hypotarsus (u).
Geronticus eremita: right coracoid in dorsal view (c), left tibiotarsus in cranial view (l). (e) Right scapula of Platalea leucorodia. Plegadis falcinellus: right tibiotarsus in cranial view (m), right tarsometatarsus in dorsal view (p), and proximal view of left hypotarsus (s).
Left tarsometatarsus of Pseudibis papillosa in dorsal (q) and proximal (v) views. (t) Right tarsometatarsus (hypotarsus) of Eudocimus
ruber in proximal view. cd, condylus dorsalis; chi, cristae hypotarsi intermediae; cid, canalis interosseus distalis; cmh, crista medialis
hypotarsi; clh, crista lateralis hypotarsi; cv, condylus ventralis; df, dorsal facet of extremitas sternalis; em, epicondylus medialis; fdl,
sulcus for m. ﬂexor digitorum longus; fhl, sulcus for musculus ﬂexor hallucis longus; fmb, fossa musculi brachialis; fmI, fossa metatarsi I; fns, foramen nervi supracoracoidei; fvd, foramen vasculare distale; ims, impressio m. sternocoracoidei; la, ligamental attachment bordering impressio m. sternocoracoidei; pf, pneumatic foramen; se, sulcus extensorius; sp, sulcus patellaris; tal, tuberculum
ancorae ligamentosa; tcl, tubercle lateral to the cotyla lateralis; tdfI, tuberosity distal of fossa met. I; tic, tuberculum intercondylaris;tmg, tuberculum m. gastrocnemialis; tm II, trochlea metatarsi II; tm III, trochlea metatarsi III; tm IV, trochlea metatarsi IV; tsp, tuberculum on crista lateralis sulci patellaris; tv, tuberculum ventrale; vf, ventral facet of extremitas sternalis; vmd, deep ventromedial depression on acromion. (b, l, s, q, v) were mirrored to facilitate comparisons. (k’, r–v) are not to scale. Scale bars: 10 mm.

of P. leucorodia (see Harrison 1986 for a thoroughdiscussion of this character).
Fossa metatarsi I (Fig. 2o) is well marked in
G. pagana. In several ibises there is a distinct
tubercle distal to the fossa; this is also the case in
the fossil but not in species of Plegadis. Trochlea
metatarsi II (Fig. 2n) is more medially orientatedthan in species of Plegadis (Fig. 2p); and trochlea
metatarsi IV projects farther distally than trochlea
metatarsi II. Judging by published photographs(e.g. Mayr & Bertelli 2011, p. 234) in the Eocene
stem ibis Rhynchaeites trochlea metatarsi II projects farther distally than trochlea metatarsi IV,
which is also the case in all examined ibises withthe exception of Gerandibis, Eudocimus andspecies of Plegadis.
Phylogenetic analysis
Analysis of the character matrix in Appendix 2
resulted in a single most parsimonious tree (treelength = 90 steps, retention index = 0.76, consistency index = 0.66; Fig. 3). Monophyly of theThreskiornithidae is supported by the following
characters (unambiguous optimization of characters depicted in Fig. 3): (1) marked furrow on lateral side of maxilla, (2) schizorhinal nostrils
extending into nasofrontal hinge, (6) presence offonticuli occipitales, (11) well-developed and ventrally projecting processus paraoccipitales, (25)presence of foramen immediately below ventral
margin of facies articularis clavicularis of coracoid,(26) absence of mediolateral compression acrosstransverse plain of omal end of coracoid, (30)© 2013 British Ornithologists’ Union

absence of well-marked dorsally protruding surface
at dorsal facet of crista articularis sternalis on
coracoid, (32) tuberculum ventrale of humerus
overhanging a small pneumatic foramen, (40) circular, well-developed and elevated tuberculum m.
gastrocnemialis at distal end of femur, (41) tuberculum intercondylaris at distal end of tibiotarsus
only moderately developed and (51) large andslit-shaped foramen vasculare distale at distal endof tarsometatarsus. Although characters (20), a
wide interorbital portion of the frontal, and (22),tiny caudal fenestrae of mandible, were optimized
as synapomorphic for Threskiornithidae, thesecharacters were reversed to the plesiomorphic condition in the clade comprising Gerandibis, Eudocimus and species of Plegadis. Character (27), thepresence of foramen nervi supracoracoidei, wasoptimized as an apomorphy of Threskiornithidae;
however, this condition is likely to be plesiomorphic for neornithine birds (Mayr 2002b).
A sister group relationship between T. aethiopicus and the two species of Platalea used in theanalysis received high bootstrap support and is
supported by the following characters: (5) tip ofprocessus postorbitales projecting slightly laterally,(9, 10) long and mediolaterally narrow processus
paraoccipitales with strong ventrolateral projection,(35) ulna with very shallow depressio radialis and(48) a widely open hypotarsal sulcus for tendon of
musculus ﬂexor digitorum longus.
A clade including all other ibises is supportedby the following characters: (8) occiput occupying about or less than two-thirds of the skull in
occipital view, (24) medial aspect of acromion

Early Miocene ibis and phylogeny of Threskiornithidae

553

Figure 3. Most parsimonious tree (length = 90, consistency index = 0.66, retention index = 0.76) resulting from the analysis of thecharacter matrix in Appendix 2 and showing interrelationships of the Threskiornithidae. Apomorphies are listed on the internodes(numbers refer to characters listed in Appendix 1); only unambiguously optimized synapomorphies are shown. Filled circles represent
strict apomorphies, open circles homoplastic ones. Bootstrap values are provided below the braches; values under 60 are not shown.
Distribution of threskiornithid taxa used in this study is noted to the right. C, cosmopolitan; NW, New World; OW, Old World.

(scapula) with deep ventromedial depression,(28) ligamental attachment at mid-shaft of coracoid and (54) presence of well-developed tubercle distal to fossa metatarsi I (not present in
Eudocimus and Plegadis). Within this clade, twogroups, one encompassing the Old World ibises
and the other made up of predominantly New
World ibises, were recovered. The ﬁrst clade
includes the genera Lophotibis, Bostrychia, Geronticus and Pseudibis. Although this clade did notreceive high bootstrap support (< 60%), it isnevertheless characterized by two characters: (4)shallow fossae temporales and (13) processus
maxillopalatinus fused with os palatinum, the latter character being a derived feature for thisclade. Within this clade, L. cristata was recoveredas the sister taxon to all remaining members.
Characters (8), occiput occupying less than
two-thirds of the skull, and (31), presence ofwell-developed tuberculum on margo medialis ofextremitas sternalis of coracoid, were recovered
as apomorphies of the clade including Bostrychia,
Geronticus and Pseudibis. The close relationshipbetween Geronticus and Pseudibis received low
bootstrap support and is supported by a single
character: (28) ligamental attachment on dorsalside of shaft of coracoid not situated at mid-shaft
but towards the sternal end.

A predominantly New World clade, including
G. pagana, is statistically well supported andcharacterized by (12) an in ventral view short rostrocaudal fusion of the palatines, (29) dorsal facetof crista articularis sternalis overhanging ventral
facet (coracoid) and (34) a moderately deep fossa
musculi brachialis of the humerus. Within thisclade, T. melanopis was recovered as a sister taxon
to G. pagana, E. ruber and the two species of Plegadis. The latter clade, which also received highbootstrap support, is characterized by (5) relatively
large fonticuli occipitales, (16) rostral-most portionof bill mediolaterally wider than or as wide as
mid-portion of bill, (18) large fonticuli orbitocraniales, (20) interorbital region of frontal withstrongly notched orbital rims, (22) mandible withlarge caudal fenestrae, (42) epicondylus medialis
of tibiotarsus not well developed and (55) tarsometatarsus with trochlea metatarsi IV projecting
farther distally than trochlea metatarsi II. A close
relationship between E. ruber and species of Plegadis is supported by (9, 10) long, narrow and ventrally protruding processus paraoccipitales, (44)hypotarsus mediolaterally narrow, (46) crista medialis hypotarsi and crista lateralis hypotarsi extending plantarly to about the same level, (47)
hypotarsus with poorly developed crista lateralis
hypotarsi and shallow sulcus for musculus ﬂexor© 2013 British Ornithologists’ Union

554

V. L. De Pietri

hallucis longus and (54) absence of well-developed
tubercle distal to fossa metatarsi I.
DISCUSSION
G. pagana is the earliest record of an ibis that canbe unambiguously assigned to crown group Threskiornithidae. This work constitutes the ﬁrst osteological analysis aimed at clarifying the phylogenetic
relationships of this Early Miocene ibis within theThreskiornithidae. As such, these results also allow
for an evaluation of the interrelationships within
members of this family. Comparisons between the
results presented herein and the few molecularbased phylogenies published to date (e.g. Sibley &Ahlquist 1990, Chesser et al. 2010, see Fig. 4)
reveal both differences and similarities.
A basal divergence of the Threskiornithidae
based on bill morphology into subfamilies Threskiornithinae (ibises) and Plataleinae (spoonbills) has
been disproved by previous studies, and the present results agree with those obtained from DNA–DNA hybridization data (Sibley & Ahlquist 1990)
and recent molecular-based phylogenies (Chesser
et al. 2010) in that spoonbills are nested within
Threskiornithidae and are the sister taxa to speciesof Threskiornis (Figs 3 and 4). This relationshipmay also be supported by spoonbills and species ofThreskiornis having a similar breeding plumage
with ornamental feathers (Matheu & del Hoyo
1992). Cases of hybridization in captivity between
species of Platalea and Threskiornis have beenreported (Matheu & del Hoyo 1992, McCarthy2006), as well as between species of Eudocimus
and Platalea (McCarthy 2006).
Although phylogenetic inferences based on
DNA–DNA hybridization (Sibley & Ahlquist(a)1990) have attracted criticism (Harshman 1994),
results are in agreement with phylogenies based onmolecular sequence data (Chesser et al. 2010,
Krattinger 2010) in that the basal split within Threskiornithidae resulted in two major clades, a New
World clade comprising Neotropical taxa such as
Theristicus, Phimosus and Eudocimus, and an Old
World clade. This basal divergence was not supported in this study, and in fact the clade comprising species of Threskiornis and Platalea wasrecovered in a sister-group relationship to all
remaining ibises. Nevertheless, a New World/Old
World pattern for extant taxa to the exclusion ofThreskiornis and Platalea did result from the osteological phylogeny presented here (Fig. 3). A clade
comprising taxa that are Old World in distribution(Lophotibis, Bostrychia, Geronticus and Pseudibis) is
supported by the fusion of the os palatinum andthe processus maxillopalatinus, a feature absent in
all remaining examined taxa. L. cristata was recovered in a basal position within this clade based onfeatures of the skull (cranium not as tall is in othertaxa within this clade) and coracoid (absence of awell-developed tuberculum ancorae ligamentosa on
the margo medialis of extremitas sternalis, which ispresent in all other examined Old World taxa).
A predominantly New World clade includes
T. melanopis, the fossil ibis G. pagana, E. ruber
and species of the genus Plegadis. Within thisclade, G. pagana and P. falcinellus are found outside the Neotropics, the latter having attained anearly cosmopolitan distribution. Characters optimized as apomorphies of this clade include , inventral view, a short rostrocaudal fusion of the palatines, a dorsal facet of the extremitas sternalis of
the coracoid overhanging the ventral facet and amoderately deep fossa musculi brachialis; a basal(b)Figure 4. Previous hypotheses on the phylogeny of Threskiornithidae. (a) Tree based on DNA–DNA hybridization data (Sibley & Ahlquist 1990, see ﬁg. 367). (b) Estimated phylogeny based on mitochondrial sequence data (Chesser et al. 2010); tree was simpliﬁed
to facilitate comparisons. C, cosmopolitan; NW, New World; OW, Old World.

© 2013 British Ornithologists’ Union

Early Miocene ibis and phylogeny of Threskiornithidae

position of T. melanopis within this clade is supported by the absence of several presumably
derived features of the skull and tarsometatarsus
that are present in the remaining members of thisclade, and indeed T. melanopis bears an overall
resemblance to members of the Old World clade
in several skeletal elements.
The Early Miocene ibis G. pagana was recoveredas the sister taxon to the clade consisting of E. ruber
and species of Plegadis (Fig. 3). Osteological similarities between G. pagana and members of theextant genera Eudocimus and Plegadis had alreadybeen noticed by several authors (e.g. MilneEdwards 1867–1871, Olson 1981, Cheneval 1984),
which resulted in G. pagana being listed underboth these genera in the past (Brodkorb 1963, Olson 1981, Cheneval 1984). Indeed, species of Plegadis and Eudocimus are remarkably similar in theirosteology, particularly in features of the skull andtarsometatarsus, and as suggested by Olson (1981),
these taxa are probably closely related, a view also
supported by the phylogeny presented here.
The placement of species of Plegadis within thisNew World clade, however, has been questioned
by DNA–DNA hybridization data (Sibley & Ahlquist 1990) and by a recent study of threskiornithid
phylogeny based on mitochondrial and nuclear data
(Krattinger 2010). Both these studies suggest thatspecies of Plegadis may be more closely related to
Old World taxa than to members of the New
World clade, including Eudocimus. Although separation of species of Plegadis and Eudocimus in different clades may seem surprising given their striking
osteological similarity, the possibility that thefeatures recovered as synapomorphic for membersof both these genera (see Fig. 3) are indeed plesiomorphic for Threskiornithidae cannot be ruled out
at present. In the absence of a well-supported andcongruent placement of Plegadis in phylogenetic
analyses, this hypothesis remains conjectural. Perhaps more clarity concerning character polarity will
be gained once well-preserved specimens of putative Palaeogene stem ibises (Mayr 2002a, Mayr &Bertelli 2011, Smith et al. 2013) are evaluated in aphylogenetic context of extant Threskiornithidae.
Based on the data presented, placement of
G. pagana in the extant genus Plegadis is no longer
justiﬁed. Olson (1981) referred the Early Miocene
ibis from France to the extant genus Plegadis basedon a single feature of the tarsometatarsus, namely
the presence of a conspicuous dorsal opening of
canalis interosseus distalis (Fig. 2; see also Olson

555

1981, ﬁg. 1, p. 166). This feature, as observed in
G. pagana (see also Harrison 1986), is also present
in other ibises apart from species of Plegadis, suchas in a specimen of B. hagedash and in somespecimens of P. leucorodia. Although based on
osteological characters, G. pagana and members ofPlegadis appear to be closely related, differences
between the two, particularly regarding the tarsometatarsus, had already been noticed by several
authors (Milne-Edwards 1867–1868, Cheneval
1984, Harrison 1986) and are corroborated in thisstudy. Referral of the Saint-Gerand ibis to a new
genus corroborates recent evidence that, contrary
to the original and previous taxonomic assessments(e.g. Milne-Edwards 1867–1871, Cheneval 1984),
very few fossil taxa from the Saint-Gerand-le-Puy
area are consistently retained within extant genera(De Pietri et al. 2011a, De Pietri & Mayr 2012).
Biogeographical inferences depend upon robust
and congruent phylogenetic hypotheses. The uncertainty that stems from the discrepancy between
phylogenetic estimates obtained from molecularand morphological data, and the spurious record ofstem ibises, makes inferences on the origins of thefamily difﬁcult to assess, and whether crown groupthreskiornithids originated in the New World or the
Old World is unclear based on the evidence athand. A close relationship between taxa present in
the Aquitanian of France and birds now restricted
to sub-Saharan Africa is known for several groups(e.g. Cheneval 1989, Mayr 2011). A similar correlation between the Early Miocene European avifauna
and New World taxa has been proposed (MourerChauvire 2000) and the presence of an ibis in the
Early Miocene of France closely related to Neotropical taxa strengthens these observations. A thoroughassessment of the relationships of some Early Miocene taxa of Europe will perhaps in the future shedlight on the biogeographical signiﬁcance of the
Aquitanian avifauna of the Saint-Gerand-le-Puy
area.
I am grateful to M. Schweizer (Natural History Museum
Bern, Switzerland), L. Costeur (NMB) , R. Winkler(NMB) and P. Scoﬁeld (Canterbury Museum, New Zealand) for helpful comments and discussions during the
preparation of the manuscript, and to G. Mayr (SMF) for
comments and access to extant specimens. I thank C.
Mourer-Chauvire (FSL) , C. Sagne and R. Allain(MNHN) for providing access to fossil specimens, and T.
H. Worthy (University of Flinders) for commenting on an
early version of the manuscript. I am also grateful to F.
Krattinger and C. Haag (University of Fribourg, Switzer-© 2013 British Ornithologists’ Union

556

V. L. De Pietri

land) for supplying their unpublished data on threskiornithid phylogeny, and N. Smith (Howard University, Washington) for providing a manuscript in press. Commentsfrom four anonymous reviewers helped improve the manuscript. This study was supported by the Forschung undLehre fund (Natural History Museum Basel).

REFERENCES
Baumel, J.J. & Witmer, L.M. 1993. Osteologia. In Baumel,
J.J., King, A.S., Breazile, J.E., Evans, H.E. & Vanden
Berge, J.C. (eds) Handbook of Avian Anatomy: Nomina
Anatomica Avium, 2nd edn: 45–132. Cambridge, MA: Nuttall
Ornithological Club.
Brodkorb, P. 1963. Catalogue of fossil birds. Part 1(Archeopterygiformes through Ardeiformes). Bull. Fla. State
Mus. Biol. Sci. 7: 179–293.
Cheneval, J. 1984. Les oiseaux aquatiques (Gaviiformes arand-leAnseriformes) du gisements aquitanien de Saint-Ge
vision syste
 matiques. PalaeovertebrataPuy (Allier, France): re
14: 33–115.
Cheneval, J. 1989. Fossil bird study, and paleoecologicaland paleoenvironmental consequences: example from therand-le-Puy deposits (Lower Miocene, Allier,Saint-Ge
France). Palaeogeogr. Palaeoclimatol. Palaeoecol. 73:
295–309.
Cheneval, J. 2000. L’avifaune de Sansan. In Ginsburg, L.
 ne De Sansan Et Son Environnement.
(ed.) La Faune Mioce
Mem. Mus. Hist. Nat. 183: 321–388.
Chesser, R.T., Yeung, C.K.L., Yao, C.-T., Tian, X.-H. & Li,
S.-H. 2010. Molecular phylogeny of the spoonbills (Aves:
Threskiornithidae) based on mitochondrial DNA. Zootaxa
2603: 53–60.
De Pietri, V.L. & Mayr, G. 2012. An assessment of thediversity of early Miocene Scolopaci (Aves, Charadriiformes)
 rand-le-Puy (Allier, France). Palaeontology 55:
from Saint-Ge
1177–1197.
€ ntert, M. & Mayr, G. 2011a. A
De Pietri, V.L., Costeur, L., Gu
revision of the Lari (Aves, Charadriiformes) from the early rand-le-Puy (Allier, France). J. Vert.
Miocene of Saint-Ge
Paleont. 31: 812–828.
De Pietri, V.L., Manegold, A., Costeur, L. & Mayr, G. 2011b.
A new species of woodpecker (Aves; Picidae) from the early
Miocene of Saulcet (Allier, France). Swiss J. Palaeontol.
130: 307–314.
Dyke, G.J. & Walker, C.A. 2008. New records of the fossil‘waterbirds’ from the Miocene of Kenya. Am. Mus. Novit.
3061: 1–10.
Ferreira, C.D. & Donatelli, R.J. 2005. Osteologia craniana de
Platalea ajaja (Linnaeus) (Aves, Ciconiiformes), comparadacies de Threskiornithidae. Rev. Bras. Zool.
com outras espe
22: 529–551.
Goloboff, P.A. 1993. NONA version 2.0. Argentina: S. M. den.
TucumaHarrison, C.J.O. 1986. A re-examination of some Tertiary oldworld ibises Threskiornithidae. Tertiary Res. 7: 139–143.
Harrison, C.J.O. & Walker, C.A. 1976. Birds of the British
upper Eocene. Zool. J. Linn. Soc. 59: 323–351.
Harshman, J. 1994. Reweaving the tapestry: what can welearn from Sibley and Ahlquist (1990)? Auk 111: 377–
388.

© 2013 British Ornithologists’ Union

Hou, L.H. 1982. New form of the Threskiornithidae from theupper Eocene of the Minggang, Henan. Vertebrat.
PalAsiatic. 20: 196–202.
Krattinger, F. 2010. Molecular Phylogeny of Threskiornithidae.
MS Thesis in Ecology and Evolution, University of Fribourg,
Switzerland.
Livezey, B.C. & Zusi, R.L. 2006. Higher-order phylogeny ofmodern birds (Theropoda, Aves: Neornithes) based oncomparative anatomy. I. Methods and characters. Bull.
Carnegie Mus. Nat. Hist. 37: 1–544.
Livezey, B.C. & Zusi, R.L. 2007. Higher-order phylogeny ofmodern birds (Theropoda, Aves: Neornithes) based oncomparative anatomy. II. Analysis and discussion. Zool. J.
Linn. Soc. 149: 1–95.
Lydekker, R. 1891. Catalogue of the Fossil Birds in the British
Museum (Natural History). London: British Museum (Natural
History).
Matheu, E. & del Hoyo, J.1992. Family Threskiornithidae. In
del Hoyo, J., Elliott, A. & Sargatal, J. (eds) Handbook of the
Birds of the World, Vol. 1: 472–506. Barcelona: Lynx
Edicions.
Mayr, G. 2002a. A contribution to the osteology of the Middle
Eoceneibis
Rynchaeites
messelensis(Aves:
Threskiornithidae: Rynchaeitinae nov. subfam.). N. Jb. Geol.
€ ontol. Mh. 8: 501–512.
Pala
Mayr, G. 2002b. On the osteology and phylogenetic afﬁnitiesof the Pseudasturidae – Lower Eocene stem-grouprepresentatives of parrots (Aves, Psittaciformes). Zool. J.
Linn. Soc. 136: 715–729.
Mayr, G. 2009. Paleogene Birds. Heidelberg: Springer.
Mayr, G. 2011. Two-phase extinction of ‘Southern Hemispheric’birds in the Cenozoic of Europe and the origin of the
Neotropic avifauna. Palaeodiv. Palaeoenv. 91: 325–333.
Mayr, G. & Bertelli, S. 2011. A record of Rhynchaeites (Aves,
Threskiornithidae) from the early Eocene of the Fur
Formation of Denmark, and the afﬁnities of the allegedparrot Mopsitta. Palaeodiv. Palaeoenv. 91: 229–236.
Mayr, G. & Clarke, J. 2003. The deep divergences ofneornithine birds: a phylogenetic analysis of morphologicalcharacters. Cladistics 19: 527–553.
McCarthy, E.M. 2006. Handbook of Avian Hybrids of theWorld. New York: Oxford University Press.
Miller, A.H. & Bowman, R.I. 1956. Fossil birds of the late
Pliocene of Cita Canyon, Texas. Wilson Bull. 68: 38–46.
Milne-Edwards, A. 1868. Recherches Anatomiques et ontologiques pour Servir a l’Histoire des OiseauxPale
Fossiles de la France. Paris: Masson, 1, 1867–1868: 472 p.;
2, 1869–1871: 627 p.; atlas, 1: pl. 1–96, 2: 97–200.
 , J. 2002. Cenozoic Birds of the World, Part 1:
Mlıkovsky
Europe. Prague: Ninox Press.
, C. 2000. A new species of Ameripodius
Mourer-Chauvire(Aves: Galliformes: Quercymegapodiidae) from the lower
Miocene of France. Palaeontology 43: 481–493.
Nixon, K.C. 2002. WinClada, version 1.00.08. Ithaca, NY:.
published by the author.
Olson, S.L. 1981. The generic allocation of Ibis pagana MilneEdwards, with a review of the fossil ibises (Aves:
Threskiornithidae). J. Vert. Paleontol. 1: 165–170.
Peters, D.S. 1983. Die ‘Schnepfenralle’ Rhynchaeites
messelensis Wittich 1898 ist ein Ibis. J. Ornithol. 124: 1–27.
Richmond, C.W. 1917. Generic names applied to birds during
the years 1906 to 1915, inclusive, with additions andEarly Miocene ibis and phylogeny of Threskiornithidae

corrections to Waterhouse’s ‘Index Generum Avium’. Proc.
Natl Acad. Sci. USA 53: 565–636.
 ne infe rieur
Roux, T. 2002. Deux fossiles d’oiseaux de l’Oligoce
du Luberon. Courr. Sci. Parc. Nat. Reg. Luberon 6: 38–57.
Scoﬁeld, R.P., Worthy, T.H. & Tennyson, A.J.D. 2010. A
heron (Aves: Ardeidae) from the early Miocene of St
Bathans Fauna of Southern New Zealand. In Boles, W.E. &Worthy, T.H. (eds) Proceedings of the VII International
Meeting of the Society of Avian Paleontology and Evolution.
Rec. Aust. Mus. 62: 89–104.
Sharpe, R.B. 1899. A Handlist of the Genera and Species ofBirds, 1st edn. London: British Museum (Natural History).
Sibley, C.G. & Ahlquist, J.E. 1990. Phylogeny andClassiﬁcation of Birds – A Study in Molecular Evolution.
New Haven: Yale University Press.
Smith, N. 2010. Phylogenetic analysis of Pelecaniformes (Aves)
based on osteological data: implications for waterbird
phylogeny and fossil calibration studies. PLoS ONE 5: e13354.
Smith, N., Clarke, J. & Grande, L. 2013. A new species ofThreskiornithidae-like bird (Aves, Ciconiiformes) from theGreen River Formation (Eocene) of Wyoming. J. Vert.
Paleontol. 33: 363–381.
Stidham, T.A., Holroyd, P.A., Gunnell, G.F., Ciochon, R.L.,
Tsubamoto, T., Egi, N. & Takai, M. 2005. An ibis-like bird
(Aves: Threskiornithidae) from the late Middle Eocene of
Myanmar. Contrib. Mus. Paleontol. Univ. Mich. 31: 179–184.
Worthy, T.H., Worthy, J.P., Tennyson, A.J.D. & Scoﬁeld,
R.P. In Press. A botaurine heron (Aves: Ardeidae) from theearly Miocene of New Zealand. Paleontol. J.
Received 17 December 2012;
revision accepted 12 April 2013.
Associate Editor: Martin Collinson.

APPENDIX 1
Description of characters used in thephylogenetic analysis
1. Skull, os maxillare, marked furrow on lateralside of maxilla (nasal groove) extending distally from osseous narial opening: absent (0);present but faint (1); present and wellmarked (2). Modiﬁed from Smith (2010),
character 6.
2. Skull, schizorhinal nostrils extending into
nasofrontal hinge: no (0), yes (1).
3. Skull, conspicuous frontonasal suture: yes(0), no (1). See also Ferreira and Donatelli(2005). Yes in outgroup and Platalea..
4. Skull, fossa temporalis: deep (e.g. Ciconia,
Ardea) to moderately deep (Fig. 1e), reaching towards midline of cranium (0), very
shallow (1).
5. Skull, tip of processus postorbitalis (Fig.1e):
not as follows (0), projecting slightly laterally(1) (Fig. 1i).

557

6. Skull, occipital region, fonticuli occipitales,(Fig. 1f): absent (0); proportionally small (1);relatively large, over 2/3 of foramen magnum(2). States 1 and 2 have been observed inindividuals of Platalea leucorodia (Fig. 1i).
7. Skull, occipital region, prominentia cerebellaris: not as follows (0); with very prominent, dome-like bulge in dorsal view (1)(Fig. 1c). The prominentia cerebellaris iswell developed in species of Ardea; however,its shape within herons does not resemble
the described condition for threskiornithids.
Within Threskiornithidae, this bulge is mostprominent in species of Plegadis.
8. Skull, occipital region: occiput (Fig. 1e–i)
occupying over two-thirds of the skull in
occipital view (0), about two-thirds of theskull (1), less than two-thirds of the skull(2). Character state 2 means that the roof ofthe cranium is particularly tall in taxa forwhich this state was coded.
9. Skull, processus paraoccipitalis (Fig. 1g), longand mediolaterally narrow in occipital view:no (0); yes, ventrally projecting to aboutlevel of processus parasphenoidalis (1); yes,with strong ventrolateral projection (2).
10. Skull, lateral view, processus paraoccipitalis
narrow (as opposed to dorsoventrally
broad): no (0), yes (1).
11. Skull, well-developed and ventrally projecting processus paraoccipitalis, set off fromdorsal wall of tympanic cavity: no (0), yes(1). As described, this character is absent inCiconia and Ardea. See also Ferreira andDonatelli (2005).
12. Skull, ventral view, rostrocaudal fusion ofossa palatina at midline: long (0), short (1)(Fig. 1m–o).
13. Skull, processus maxillopalatinus fused withos palatinum: no (0), yes (1) (Fig. 1j,l).
14. Skull, ventral view, concavitas palatis deep
and pierced (Fig. 1m–o): yes (0), no (1).
15. Skull, os palatinum, pars choanalis very
deep dorsoventrally: yes (0), no (1). From
Smith (2010), character 17.
16. Skull, rostral-most portion of bill in ventral
view (Fig. 1p–q): very narrow (0); mediolaterally wider than or as wide as mid-portionof bill (1); greatly expanded (2).
17. Skull, short and oval narial openings: no(0), yes (1). This character is an autapo-© 2013 British Ornithologists’ Union

558

V. L. De Pietri

morphy of Plataleinae; see Ferreira andDonatelli (2005).
18. Skull, fonticuli orbitrocraniales (Fig. 1j–k),
caudal of lacrimal duct: absent or small (0);large (1). Fonticuli are absent in Ciconia.
19. Skull, orbital foramen (Fig. 1j–k) occupying
most of interorbital septum: no (0), yes (1).
See also Ferreira and Donatelli (2005).
20. Skull, frontal at interorbital region, orbital
rims (Fig. 1b) strongly notched: yes (0), no(1).
21. Skull, fusion of os frontale and os lacrimale:yes (0), no (1).
22. Mandible, caudal fenestrae (Fig. 1r,s): present and large (0), absent or tiny (1).
23. Scapula, robust, mound-shaped tuberosity
present on the lateral surface of the scapula: present (0), absent (1). After Smith(2010), character 160.
24. Scapula, acromion, medial aspect, deep ventromedial depression (Fig. 2d): no (0), yes(1).
25. Coracoid, extremitas omalis, medial aspect,sulcus musculi supracoracoideus, pneumaticforamina penetrating acrocoracoid: no (0),yes (1). Worthy et al. (in press), character
22; modiﬁed from Scoﬁeld et al. (2010),
character 17.
26. Coracoid, extremitas omalis, medial aspect.
Processus acrocoracoideus and supracoracoideal sulcus–mediolateral compression
across the transverse plain: moderately compressed (0), weakly or not compressed (1).
Modiﬁed from Scoﬁeld et al. (2010), character 18.
27. Coracoid, foramen nervi supracoracoidei(Fig. 2b): present (0), absent (1). Although
this foramen is absent in Ciconia ciconia, it
was reported as present in Leptoptilos(Mayr & Clarke 2003).
28. Coracoid, shaft, dorsal aspect, ligamental
attachment bordering impressio m. sternocoracoidei at mid-shaft (Fig. 2a,c): no (0),yes (1).
29. Coracoid, extremitas sternalis, dorsal aspect:ventral facet of crista articularis sternalis
extending farther sternally than dorsal facet(0) (Fig. 2b); dorsal facet overhanging ventral facet (1) (Fig. 2c).
30. Coracoid, extremitas sternalis, dorsal aspect.
Presence of well-marked, dorsally protruding surface at dorsal facet of crista articularis© 2013 British Ornithologists’ Union

sternalis, lateral to angulus medialis: yes (0),no (1).
31. Coracoid, extremitas sternalis, ventromedialaspect. Well-developed and angular tubercle(tuberculum ancorae ligamentosa, sensu Livezey and Zusi (2006): character 1302; seealso Smith (2010), character 183) on margo
medialis of extremitas sternalis (Fig. 2a): no(0), yes (1). Shape and degree of development varies within threskiornithids.
32. Humerus, proximal end, caudal surface. Tuberculum ventrale overhanging a relatively
small pneumatic foramen, so that it is notcompletely visible in caudal view (Fig. 2g):
no (0), yes (1). Within Threskiornithidae,
this feature is only absent in Geronticus eremita.
33. Humerus, distal end, cranial view: condylus
dorsalis projecting only slightly more distallythan condylus ventralis (i.e. almost at samelevel) (0); condylus ventralis distinctly moredistally situated than condylus dorsalis (1)(Fig. 2f).
34. Humerus, distal end, cranial surface, fossa
musculi brachialis (Fig. 2f): shallow (0),moderately deep (1).
35. Ulna, distal end, ventral view, marked depressio radialis: yes (0); no, i.e. very shallow(1).
36. Carpometacarpus, fovea carpalis cranialis:shallow (0), deep (1). Modiﬁed from Smith(2010). See also Livezey and Zusi (2007),
character 1647.
37. Carpometacarpus, proximodistal extent ofsulcus tendineus on dorsal surface of metacarpal II: sulcus extending across length ofmetacarpal II (0), sulcus limited to distal
half of metacarpal II (1). Modiﬁed from
Smith (2010), character 276. See also Livezey and Zusi (2007), character 1603.
38. Femur, proximal end, rounded pneumaticforamen on craniomedial side of trochanter
femoris: absent (0), present (1). Modiﬁed
from Smith (2010). See also Livezey andZusi (2007), character 1976.
39. Femur, distal end, lateral view, well-marked
tubercle on crista lateralis sulci patellaris,
proximal of sulcus patellaris (Fig. 2j): no(0), yes (1).
40. Femur, distal end, circular, well-developedand elevated tuberculum for m. gastrocnemialis (Fig. 2i): no (0), yes (1).

Early Miocene ibis and phylogeny of Threskiornithidae

559

digitorum longus (occupying most of the
hypotarsus): yes (0), no (1).
49. Tarsometatarsus, corpus metatarsi, shape of
medial margin of tarsometatarsal shaft at its
proximal extent: rounded, similarly conformed as rest of shaft (0); compressed
dorsoplantarly, relatively thin and/or crestlike (1). From Smith (2010), character 429.
See also Livezey and Zusi (2007), character
2288.
50. Tarsometatarsus, shaft, plantar aspect, crista
plantaris lateralis in proximal half: weakly
developed (0), strongly developed (1).
Modiﬁed from Scoﬁeld et al. (2010), character 13, and Worthy et al. (in press), character 17.
51. Tarsometatarsus, distal end, dorsal aspect,size and shape of distal foramen: small andcircular (0), large and slit shaped (1). Modiﬁed from Scoﬁeld et al. (2010), character 4.
52. Tarsometatarsus, distal end, dorsal aspect.
Conspicuous dorsal opening of canalis
interosseus distalis (Fig. 2n,p): no (0), yes(1). This condition is variable within Threskiornithidae.
53. Tarsometatarsus, distal end, mediolaterallycompressed trochlea, with trochlea metatarsi II more plantarly positioned (Fig. 2p):
no (0), yes (1).
54. Tarsometatarsus, distal end, plantar view,
tubercle distal to fossa metatarsi I (Fig. 2o):absent or poorly developed (0), conspicuous, well-developed (1).
55. Tarsometatarsus, distal end, dorsal view.
Trochlea metatarsi IV projecting farther
distally than trochlea metatarsi II (Fig. 2q):
no (0), yes (1). In Platalea leucorodia tr.
met. IV projects only slightly more plantarly past tr. met. II.

41. Tibiotarsus, distal end, cranial view; very
well-developed tuberculum intercondylaris(Fig. 2m): yes (0), no (1).
42. Tibiotarsus, distal end, cranial view, welldeveloped epicondylus medialis (Fig. 2k):
yes (0), no (1). The epicondylus medialis isparticularly well-developed and medially
protruding in Geronticus eremita, whereas itis essentially absent in Gerandibis, Eudocimus and Plegadis falcinellus.
43. Tarsometatarsus, proximal view. Relative
development of tuberositas ligamentum
collateralis lateralis: substantially developed, rounded tubercle on the dorsolateralborder of the proximal tarsometatarsus,
just below the cotylar rim (0); indistinct toweakly developed tuberosity or fovea (1).
Modiﬁed from Smith (2010), character
415. See also Livezey and Zusi (2007),
character 2255.
44. Tarsometatarsus, proximal view, hypotarsus(plantar to cotylae) mediolaterally narrow(Fig. 2r–v): yes (0), no (1).
45. Tarsometatarsus, hypotarsus with medially
positioned sulcus hypotarsi: no (0), yes (1).
46. Tarsometatarsus, hypotarsus, crista medialis
hypotarsi and crista lateralis hypotarsi
extending plantarly to about the same level(0) (Fig. 2t); crista medialis hypotarsi protruding farther plantarly than crista lateralis
hypotarsi (1) (Fig. 2r).
47. Tarsometatarsus, hypotarsus, prominentcrista lateralis hypotarsi separated from cristae hypotarsi intermediae by well-marked
sulcus for musculus ﬂexor hallucis longus(Fig. 2u): yes (0), no (1). Not applicablefor Ciconia and Platalea.
48. Tarsometatarsus, hypotarsus, widely open
sulcus for tendon of musculus ﬂexor
APPENDIX 2

Character matrix of 55 osteological characters used for the phylogenetic analysis.
A = (01); B = (12)
1

10

20

30

40

50

Ciconia_ciconia
0000000000000000000000000010000000000100000000?00000000
Ardea_cinerea
1000000000001010011010100010000010011010011101011100000
Gerandibis_pagana
211002010011001?01001?11110111111101101111110101111A011© 2013 British Ornithologists’ Union

560

V. L. De Pietri

Plegadis_falcinellus
2110021111110111010010111101110110011001011010111111101
Plegadis_ridgwayi
2110021111110111010010111101110110011001001010111111101
Eudocimus_ruber
2110020111110011010010111101110111011001111000111110001
Geronticus_eremita
2111010200101010000111111100011010011001101101011110010
Pseudibis_papillosa
2111010200101010000111111100011110011101101101011110010
Bostrychia_hagedash
2110020200101010000111111101011110011001101101011111010
Lophotibis_cristata2111010100101010000111111101010110011001101111011110010
Theristicus_melanopis
2110010100110010000111111101110111011001101101011110010
Threskiornis_aethiopicus
2110110021100011010111101100010110111001101101001110000
Platalea_leucorodia
21011B0021100012110111101100010110111001101101?0111A101
Platalea_ajaja
2101010021100012100111101100010110?11001101101?01111000© 2013 British Ornithologists’ Union