Relationships and Evolution
of Flamingos
(Aves: Phoenicopteridae)
STORRS L. OLSON
and
ALAN FEDUCCIA
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY ? NUMBER 316
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S M I T H S O N I A N C O N T R I B U T I O N S T O Z O O L O G Y ? N U M B E R 3 1 6
Relationships and Evolution
of Flamingos
(Aves: Phoenicopteridae)
Storrs L. Olson
and Alan Feduccia
SMITHSONIAN INSTITUTION PRESS
City of Washington
1980
ABSTRACT
Olson, Storrs L., and Alan Feduccia. Relationships and Evolution of Fla-
mingos (Aves: Phoenicopteridae). Smithsonian Contributions to Zoology, number
316, 73 pages, 40 figures, 2 tables, 1980.?Previous evidence supposedly
showing a relationship between flamingos and either storks (Ciconiiformes) or
ducks (Anseriformes) is re-examined in light of the recent hypothesis deriving
flamingos from shorebirds of the order Charadriiformes. Anatomical charac-
ters used to indicate relationship between flamingos and storks are shown to
consist entirely of primitive "non-anseriform" traits found in several other
orders, including Charadriiformes. Most of the presumed anseriform charac-
ters of flamingos also occur in the Charadriiformes, as do all of the characters
of flamingos that do not occur in either Ciconiiformes or Anseriformes. The
distinctive life history and behavior of flamingos is demonstrated as being very
similar to that of the Recurvirostridae (Charadriiformes), particularly the
Australian Banded Stilt {Cladorhynchus leucocephalus), but is unlike that of storks
or ducks. The appendicular myology of Cladorhynchus is described and is found
to be quite similar to that of flamingos, whereas neither is close to storks. The
thigh muscle M. iliotibialis medialis, heretofore considered unique to flamin-
gos, was discovered in Cladorhynchus but not in other Recurvirostridae. Evi-
dence from osteology, natal down, oology, and internal parasites strongly
supports a charadriiform derivation of flamingos; pterylosis does not contra-
dict such a relationship; and knowledge of the early evolution of flamingos
and Anseriformes offers a logical explanation for their sharing similar mallo-
phagan parasites. The earliest certain flamingo, from the early Middle Eocene
of Wyoming, is described herein as a new monotypic genus and species that
was intermediate in size and morphology between the Recurvirostridae and
modern flamingos. Other aspects of paleontology of flamingos are discussed.
Evolutionary steps in the development of filter feeding in birds are outlined.
The structure of the feeding apparatus of flamingos is shown to be entirely
different from that of the Anseriformes, but is strikingly convergent towards
that of baleen whales. Morphological and behavioral precursors for filter
feeding are shown to occur in the Charadriiformes but not in the Ciconi-
iformes. Flamingos (Phoenicopteridae) clearly belong in the order Charadri-
iformes, suborder Charadrii, immediately following the Recurvirostridae.
OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recorded
in the Institution's annual report, Smithsonian Year. SERIES COVER DESIGN: The coral Montastrea
cavemosa (Linnaeus).
Library of Congress Cataloging in Publication Data
Olson, Storrs L
Relationships and evolution of flamingos (Aves, Phoenicopteridae)
(Smithsonian contributions to zoology ; no. 316)
Bibliography: p.
1. Flamingos?Evolution. 2. Flamingos?Classification. 3. Birds, Fossil. 4. Birds?Evolu-
tion. 5. Birds?Classification. I. Feduccia, J. Alan, joint author. II. Title. III. Series:
Smithsonian Institution. Smithsonian contributions to zoology ; no 316
QL1.S54 no. 316 [QL696.C56] 591s [598'.34] 80-607058
Contents
Page
Introduction 1
Acknowledgments 3
Review of Previous Anatomical Information 3
Life History and Behavior 9
Myology 15
Appendicular Myology of Cladorhynchus 17
Pterylosis 31
Natal Down 34
Oology 34
Parasitology 36
Biochemistry 39
Osteology 39
Skull 39
Postcranial Skeleton 40
Paleontology 43
A New Stilt-like Flamingo from the Middle Eocene of Wyoming 47
Order CHARADRIIFORMES Huxley, 1867 48
Suborder CHARADRII Huxley, 1867 48
Family PHOENICOPTERIDAE Bonaparte, 1831 48
Juncitarsus, new genus 48
Juncitarsus gracillimus, new species 48
Aspects of Evolution of Filter Feeding 58
Conclusions 66
Literature Cited 69
111

Relationships and Evolution
of Flamingos
(Aves: Phoenicopteridae)
Storrs L. Olson
and Alan Feduccia
Introduction
The living flamingos (Phoenicopteridae) con-
stitute a small and easily recognized group of four
to six species of large, brightly colored waterbirds
with extremely long legs and neck and a uniquely
shaped bill adapted for filter-feeding. They are
colonial and characteristically inhabit highly sa-
line bodies of shallow water. The existing species
are placed in three genera that are separable into
two groups on bill morphology: (1) Phoenicopterus,
which has a more primitive filtering apparatus,
and (2) Phoenicoparrus and Phoeniconaias, which are
more specialized (Jenkin, 1957). The last two
genera are separated from each other only by the
presence or absence of the hind toe, which is very
reduced in flamingos in any case, so that contin-
ued recognition of the genus Phoeniconaias is prob-
ably unwarrented. We have not detected char-
acters of generic value in the postcranial skeleton
that will separate the two groups differing in
feeding adaptations. For purposes of extrafamilial
comparisons, modern flamingos can be regarded
as essentially monogeneric, although we have
Storrs L. Olson, Department of Vertebrate Zoology, National Museum
of Natural History, Smithsonian Institution, Washington,
DC. 20560. Alan Feduccia, Department of Zoology, University
of North Carolina, Chapel Hill, North Carolina 27514.
made no innovations in generic usage in the
present paper.
The proper phylogenetic position of the Phoen-
icopteridae has long been a perplexing problem
in avian systematics. Because of the conflicting
nature of the taxonomic evidence presented so
far, the relationships of these birds have never
been satisfactorily resolved. Flamingos are most
often placed with storks, herons, and ibises in the
order Ciconiiformes. This assemblage consists of
large, long-legged waterbirds having a long neck,
"desmognathous" palate, and usually altricial
young. Olson (1979) has recently suggested that
the order may be an entirely artificial collection
of unrelated families. The association of flamin-
gos with storks and their supposed allies was
probably made originally solely on the basis of
their large size and general proportions. This
allocation was later "supported" by a body of
evidence that we shall show to be altogether
fallacious.
Other workers noted that the lamellate bill,
webbed feet, mallophagan parasites, and some
general aspects of the behavior of flamingos
seemed to point toward a relationship with ducks
and geese (Anseriformes). Controversy has sub-
sequently centered on whether flamingos are
more closely related to the storks or to the ducks.
1
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
Continual equivocation has resulted in some au-
thors elevating the flamingos to an order of their
own (Phoenicopteriformes), an action that merely
avoids the question of relationships.
All comparisons of flamingos have traditionally
been made with Ciconiiformes on one hand and
Anseriformes on the other, but as we shall see,
most of the characters cited as showing relation-
ship also occur outside those two groups. Many
of the supposed ciconiiform characters of fla-
mingos are really only negative characters that
are simply "non-anseriform" in nature and not
really indicative of relationship to storks. Char-
acters of flamingos that are shared with both
Anseriformes and Ciconiiformes have even been
cited by some authors as evidence of a common
origin of all three groups, despite the fact that
these characters are likewise found in birds of
several other orders.
The first alternative to the ciconiiform-anseri-
form hypothesis of flamingo relationships was
advanced by Feduccia (1976), who proposed that
flamingos are related to shorebirds (Charadri-
iformes) and have no affinity with the Ciconi-
iformes. This idea came about through studies of
the fossil bird Presbyornis (McGrew and Feduccia,
1973; Feduccia and McGrew, 1974; Feduccia,
1976, 1977a, 1977b, 1978, in press). Bones of
Presbyornis occur in great concentrations in early
Eocene deposits of the western United States and
the birds were evidently highly colonial, as are
modern flamingos. For this reason and because
Presbyornis had originally been described by Wet-
more (1926) as a new family of Charadriiformes
related to the Recurvirostridae, Feduccia (1976)
made comparisons with shorebirds. He found
both Presbyornis and the Phoenicopteridae to be
most similar in their postcranial osteology to the
Charadriiformes and very different from storks
and herons. We now know, however, that the
skull of Presbyornis is duck-like (Feduccia, 1978;
Olson and Feduccia, in press) and, apart from a
rather close similarity in the naso-frontal area, is
quite different from that of flamingos. Presbyornis
provides evidence for a charadriiform origin of
the Anseriformes (Olson and Feduccia, in press),
but similarities between Presbyornis and flamingos
may be attributable to both having been derived
from the Charadriiformes, rather than indicating
that they are closely related to each other. Nev-
ertheless, Presbyornis coincidentally pointed the
way towards the proper association of flamingos
with the Charadriiformes.
In the course of our investigations we found
that all the evidence relating to the systematics of
flamingos could be best explained by their having
a charadriiform origin. Furthermore, it soon be-
came apparent not just that flamingos were de-
rived from the Charadriiformes but that they
were derived from a particular family, the Re-
curvirostridae. In this connection we have made
repeated comparisons with the Australian
Banded Stilt, Cladorhynchus leucocephalus, an ex-
traordinary bird that shares a number of unique
traits with flamingos and which can in many
respects be regarded as forming an intermediate
between the Recurvirostridae and the Phoenicop-
teridae.
In view of our findings, we take satisfaction in
noting that in Willughby's Ornithology (Ray,
1678), which is regarded as the foundation of the
scientific study of birds, the flamingo appears in
Book III, Part II, with "birds of a middle nature
between swimmers and waders, or that do both
swim and wade" (page 312), in a separate section,
the "whole-footed [webbed] long-legged birds"
(page 320), that otherwise includes only the avo-
cet (Recurvirostra, Charadriiformes). These two
were far removed from the "cloven-footed water-
fowl" in which were placed the storks and herons.
In his Systema Naturae, Linnaeus (1758) gener-
ally followed the classification of Willughby and
Ray for birds, "and where he departed from his
model he seldom improved upon it" (Newton,
1896:8 [intro.]). Linnaeus led off his order Grallae
with the flamingos, followed immediately by
spoonbills (Threskiornithidae), certain storks (Ci-
coniidae), and the species he included in Ardea,
which was composed mainly of herons, storks,
and cranes. These were succeeded by shorebirds
and various gruiforms. The association of flamin-
gos with storks and herons, thus begun, has con-
tinued up to the present and has quite successfully
obscured the true relationships of flamingos.
NUMBER 316
Sibley, Corbin, and Haavie (1969:176) pro-
vided a comprehensive review of the classification
and relationships of flamingos, citing previous
evidence from paleontology, anatomy, parasites,
behavior, and new evidence from biochemistry,
from which they concluded that the flamingos
should be "treated as a suborder, Phoenicopteri,
in the Order Ciconiiformes and that, in a linear
list, the Anseriformes and Ciconiiformes be
placed adjacent to one another." Because their
study has come to be regarded as a standard
reference on the systematics of flamingos and has
been cited as showing proof of ciconiiform affin-
ities (e.g., Parkes, 1978), we have analyzed the
evidence they presented in critical detail, aug-
menting this with new data and evaluating the
whole in light of the charadriiform affinities first
proposed by Feduccia (1976).
ACKNOWLEDGMENTS.?Without the alacritous
cooperation of individuals and museums in Aus-
tralia, we would not have had access to some of
our most crucial and convincing evidence. For
providing information and specimens we are es-
pecially indebted to A. R. McEvey and Lorene
Reid, National Museum of Victoria, Melbourne;
Shane Parker, South Australian Museum (SAM),
Adelaide; and G. M. Storr, Western Australian
Museum, Perth. James A. McNamara generously
provided us with his unpublished manuscript on
the feeding ecology of Cladorhynchus.
Other specimens were made available to us
through the kindness of John Farrand, Jr., and
Malcolm C. McKenna, American Museum of
Natural History (AMNH), New York, and
Eleanor H. Stickney, Peabody Museum of Nat-
ural History, Yale University, New Haven. We
are grateful to Robert J. Emry and Arnold D.
Lewis for their efforts in trying to locate an
important fossil flamingo locality. Pierce Brod-
korb kindly permitted the examination of certain
fossils in his care.
Illustrations are by Sigrid K. James, Lloyd
Logan, Ellen Paige, and Jaquin B. Schulz. Pho-
tographs of specimens are the painstaking work
of Victor E. Krantz. SEM photographs of egg-
shells were prepared by Mary Jacque Mann.
Anna L. Datcher and Jean J. Smith patiently
typed several versions of the manuscript.
For discussions, information, and help in elu-
cidating a diverse variety of topics, we are in-
debted to Mary Heimerdinger Clench, K. C.
Emerson, C. Lewis Gazin, James G. Mead, Har-
old Mayfield, Kenneth C. Parkes, Franklin L.
Pearce, and Richard L. Zusi. We are particularly
grateful to James C. Vanden Berge for his exten-
sive comments on the section on myology, which
was also criticized by Robert J. Raikow. For
offering overall comments on the manuscript we
are indebted to Ernst Mayr, David W. Steadman,
and George R. Zug.
Review of Previous Anatomical Information
Sibley et al. (1969) have most recently been
cited by Parkes (1978:9) in connection with the
supposed "substantial amount of evidence . . .
gathered by earlier workers that indicates rela-
tionship of the flamingos to the Ciconiiformes"
that "would have to be disposed of satisfactorily
before serious consideration can be given to Fed-
uccia's proposed phylogeny for flamingos that
involves no relationship at all to Ciconiiformes."
In their discussion of anatomical evidence, Sibley
et al. (1969:159, table 3) present a summary of
most of the characters cited in the earlier litera-
ture on flamingo systematics (reproduced here as
Table 1). In accordance with Parkes' admoni-
tions, we have analyzed each of these.
"Characters Shared with the Ciconiiformes"
1. "(partly) nidifugous": The intention is
not clear, particularly since "nidifugous" is given
later as a character (19) shared with Anseriformes.
According to the terminology of Nice (1962), all
Ciconiiformes except flamingos are semi-altricial
(unable to leave nest, down covered, fed by par-
ents); Anseriformes are type 2 precocials (leave
nest first day or two, down covered, follow parents
but feed themselves); flamingos are semi-preco-
cial (stay at nest though able to walk, down
covered, fed by parents). Charadriiformes may be
either precocial (e.g., shorebirds) or semi-preco-
cial (e.g., gulls). Downy flamingo chicks leave the
nest within three or four days and so seem much
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
TABLE 1.?Summary of anatomical characters of flamingos reproduced exactly as in Sibley et
al. (1969, table 3) except with characters numbered to facilitate reference to the text
Characters shared with
Ciconiiformes
Characters shared with
Anseriformes
Characters shared with
both orders
Characters shared with
neither order
Developmental:
1 (partly) nidifugous
2 two coats of down
Integumental:
3 down structure
4 pterylosis
5 aftershaft present
Skeletal:
6 basipterygoid process
present
7 palatine and vomer
8 rostrum
9 pelvis
10 number ribs
Muscular:
11 flight muscle
attachment
12 gastrocnemius
Others:
13 carotid artery
arrangement
14 cervical air sacs divided
15 intestinal convolutions
16 penis rudimentary
17 abdominal air sacs large
Developmental:
18 thick down on young
19 nidifugous
Integumental:
20 feather structure
21 waterproof plumage
22 webbed feet
23 lamellate bill
Skeletal:
24 nasal aperture
25 supraorbital depression
26 lachrymals
27 quadrate
28 mandibular angle
29 pectoral girdle
Others:
30 caeca
31 tongue shape
Integumental:
32 tufted oil gland present
33 11 primaries
34 diastataxic
Skeletal:
35 carinate
36 desmognathous
37 holorhinal
38 pervious nares
39 no ectocondylar process
40 16-25 cervical vertebrae
Muscular:
41 ambiens present
Integumental:
42 reduced hallux
43 inverted bill
44 filter apparatus
Muscular:
45 flexor tendons type IV
46 1 pair syrinx muscles
47 small femoral-caudal
48 BXY + muscle formula
Other:
49 type of air cells in lung
more like the young of shorebirds or ducks than
the helpless young of Ciconiiformes. Among the
Charadrii, the young of Cladorhynchus do not leave
the nest immediately after hatching, as do those
of all other Recurvirostridae, but the degree of
parental attendance is not yet known.
2. "two coats of down": Sibley et al. (1969)
stress the fact that in young flamingos there are
two successive coats of natal down, a condition
they represent as characteristic of the Ciconi-
iformes but absent in the Anseriformes. The sit-
uation is more complicated than they indicate,
and is discussed beyond (page 34), where we
show that the condition of the natal down in
Cladorhynchus is unique in the Charadrii formes in
being like that of flamingos.
3. "down structure": Sibley et al. (1969)
cite Reichenow (1877) as noting that flamingos
have simple, unbranched down like that of Ci-
coniiformes and unlike the branched rhachidial
down of Anseriformes. The down of flamingos,
however, does not differ in this respect from the
non-rhachidial down of the Charadriiformes or
that of most other precocial birds.
4. "pterylosis": This comes ultimately from
Nitzsch's (1867:132) statement that the pterylosis
of Phoenicopterus is "perfectly Stork-like." This
came about through contrasting the pterylosis of
flamingos and storks with the highly divergent
pterylosis of herons. There is actually little simi-
larity between the pterylosis of flamingos and
storks (see page 31).
5. "aftershaft present": The aftershaft is ab-
sent or rudimentary in the Anseriformes and it is
present in flamingos and Ciconiiformes. It is also
present in the Charadriiformes and many other
NUMBER 316
orders of birds (Beddard, 1898).
6. "basipterygoid process present [sic]": This
would be interpreted as a lapsus calami if Sibley
et al. (1969:161) had not repeated that the "pres-
ence of a basi-pterygoid process" is a shared
character uniting flamingos with Ciconiiformes.
This statement may derive from Beddard's (1898:
441) erroneous assertion that the skull in Phoeni-
copterus has "basipterygoid processes, to which the
anterior ends of the pterygoids are attached." In
fact, the basipterygoid processes are invariably
absent in the Ciconiiformes and are absent or
only very rudimentary in flamingos, whereas in
the Anseriformes the so-called basipterygoid pro-
cesses are particularly large and well developed.
These processes may well not be homologous from
one group of birds to another. The basipterygoid
processes are quite variable in the Charadri-
iformes, being absent in some groups and present
in others. This character is certainly not useful for
determining the relationships of flamingos.
7. "palatine and vomer": See character 8
below.
8. "rostrum": The supposed similarity of
the palatine, vomer, and rostrum of flamingos to
those of storks seems to have been taken by Sibley
et al. from uncritical comments of Reichenow
(1877) and Gadow (1877) and may also stem in
part from Huxley's (1867:461) erroneous and un-
substantiated statement that in flamingos "the
general structure of the rostrum is quite similar
to that found in the Storks and Herons." Quite
to the contrary, the general structure of the ros-
trum of adult flamingos is not like that of any
other bird. Reichenow's (1877) paper concerns
only the Ciconiiformes, to which he had already
assumed the flamingos belonged, and he saw
similarities where none existed. Although distinc-
tive, the palate in flamingos is actually more
similar to that of shorebirds (as exemplified by
the Recurvirostridae) than that of storks (pages
39-40.
9. "pelvis": This seems to stem from a single
sentence in Gadow (1877:386), stating that the
pelvis in flamingos is purely stork-like and hardly
similar to that of ducks at all, particularly in the
features of the pubis. This is partly true, although
further comparison shows the pelvis of flamingos
to be even more similar to that in the Recurvi-
rostridae than to storks (page 41).
10. "number ribs": We have not located a
prior reference to this character but it may derive
from some of the statements of Gadow (1877),
who later stated that "from a taxonomic point of
view Ribs are valueless" (Gadow, in Newton,
1896:789). We found that flamingos may have
either 5 or 6 ribs attached to the sternum. The
same number may be found in the Charadri-
iformes, in some Ciconiiformes and Anseriformes,
and in many other orders as well (Fiirbringer,
1888).
11. "flight muscle attachment": This comes
from the observations of Weldon (1883:647).
In Storks it is well known that the pectoralis major is divided
into two or more layers, easily separable from one another,
and that its attachment to the humerus forms a tendinous
arch beneath which the brachial muscles pass from the
coracoid to the arm. In Phoenicopterus, Gadow has shown that
these features are exactly repeated; . . . I need hardly point
out that this condition is absolutely unknown among La-
mellirostres [= Anseriformes].
The "pectoralis major" (= M. pectoralis) is
known to be divided into two or three layers in
the Gruidae, Cathartidae, Procellariiformes, Pel-
ecaniformes, and Scopidae, in addition to storks
(George and Berger, 1966:307-308). Hudson et al.
(1969) describe this muscle as being divided in
the Laridae and Alcidae. We dissected specimens
of Cladorhynchus Uucocephalus and Himantopus mexi-
canus (Recurvirostridae) and found this muscle to
be distinctly divided into two sections, which are
partially coalesced along the dorsolateral margin
(page 19). The general configuration is as de-
scribed and illustrated by Weldon (1883) for
Phoenicopterus and is indeed quite distinct from the
condition we observed in a specimen of duck,
Anas poecilorhynchus. The division of this muscle in
certain storks (Leptotilos) is actually quite differ-
ent from that of flamingos (Vanden Berge, 1970).
This appears to be another character that sepa-
rates flamingos from the Anseriformes but that is
shared with numerous other orders, including the
Charadriiformes.
12. "gastrocnemius": Weldon (1883) is again
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
cited for noting that flamingos supposedly differ
from the Anatidae in having the gastrocnemius
arising by three heads instead of two and in
having the accessory semitendinosus muscle (=
M. flexor cruris lateralis pars accessoria) present.
He did not mention that in the last character
flamingos differ just as much from storks, in
which the accessory semitendinosus is also absent.
Furthermore, the gastrocnemius in at least some
Anatidae arises by three heads (Raikow, 1970:
34). The three-headed gastrocnemius and the
accessory semitendinosus occur in many birds,
including the Charadrii (George and Berger,
1966). Actually, the gastrocnemius in flamingos
has four heads (Vanden Berge, 1970), as does that
of Cladorhynchus (Figure la).
13. "carotid artery arrangement": Sibley et
al. regard Glenny's (1955) findings on the carotid
arteries as only questionably indicating a rela-
tionship between flamingos and the Ciconi-
iformes. Flamingos have type B-2-s carotid arter-
ies. Anseriformes, Charadriiformes, all Ciconiidae
and Threskiornithidae, and most Ardeidae have
type A-l carotids. A few of the Ardeidae have
type B-l carotids, Ardeola speciosa has type B-2-s,
and Botaurus lentiginosus may have either type B-1
or B-2-s. The B-2-s condition was evidently de-
rived independently from the A-l condition at
least twice within the Ardeidae. The B-2-s con-
dition in flamingos had to have been derived
independently of that in Botaurus lentiginosus and
Ardeola speciosa and it could as easily have come
from the A-l condition in shorebirds or ducks as
from the A-l condition in Ciconiiformes, a point
later specifically admitted by Sibley and Ahlquist
(1972).
14. "cervical air sacs divided": This charac-
ter, along with character 17 ("abdominal air sacs
large"), stems from Weldon's (1883) observations
that the air sacs in flamingos are in these respects
more like those of storks than ducks. In a modern
account of the air sac system of birds (Duncker,
1971), no mention is made of any peculiarities of
flamingos. The cervical air sacs are paired in most
birds and are unusually large in the Sphenisc-
idae, Anatidae, Falconidae, and Accipitridae
(Duncker, 1971:49), so it would appear that this
is but another character in which flamingos differ
from ducks but resemble many other birds. The
same is true of the large abdominal air sacs, which
are typical of most birds. According to Duncker
(1971:62) storks differ from all other birds in
having the posterior thoracic air sac divided into
medial and posterior sacs. If any conclusion can
be drawn from this it is that the air sacs of
flamingos do not seem to agree with those of
either storks or ducks.
15. "intestinal convolutions": Beddard (1898:
441) stated only that in flamingos "the intestines
are not duck-like," which carries no information
about affinities with other groups. We note from
the table in Gadow (1889) that the general intes-
tinal pattern in flamingos is found in the Cha-
radrii as well as in storks, although Gadow's
attempts to use the varying patterns of intestinal
convolutions in birds as taxonomic characters
have been largely discredited (see Sibley and
Ahlquist, 1972:21-22).
16. "penis rudimentary": This feature is of
importance only in contrast to ducks, which have
a well-developed penis. The penis is rudimentary
or lacking in most birds, including flamingos and
shorebirds, although it might be noted that Bed-
dard (1898:37) states that a penis exists in the
Ciconiiformes (he does not say in which forms)
and in Burhinus (Charadriiformes), in addition to
ratites, tinamous, cracids, and ducks.
17. "abdominal air sacs large": See character
14 above.
"Characters Shared with Anseriformes"
18. "thick down on young": Thick down is
also present in the young of Charadriiformes and
other precocial birds.
19. "nidifugous": See character 1 above.
20. "feather structure": See character 21 be-
low.
21. "waterproof plumage": To Chandler
(1916) the feather structure of flamingos was
much more similar to that of Anseriformes than
Ciconiiformes, but he did not specifically com-
pare flamingos with Charadriiformes. Sibley et
al. (1969:160) felt that the "close, hard, water-
proof nature of the plumage as a whole, shared
NUMBER 316
by flamingos and geese, could easily be the result
of convergence." They cite Rutschke (1960) as
showing that "water birds in different orders are
more alike in feather structure than non-aquatic
birds even within the same order." Nonetheless,
it is worth observing that the feathers in the
Recurvirostridae are notably close, hard, and
dense; photographs of Recurvirostra americana en-
gaged in feeding show the plumage to be quite
waterproof as well (Tremaine, 1975:75).
22. "webbed feet": Species of birds with
webbed feet occur in a variety of orders other
than Anseriformes, including the Charadri-
iformes. Within the Recurvirostridae, Recurvirostra
and Cladorhynchus have webbed feet, while Himan-
topus has only vestigial webs.
23. "lamellate bill": As detailed later (pages
59-60), the structure of the bill and lamellae in
flamingos and ducks is fundamentally different
and is not indicative of relationship.
24. "nasal aperture": This character and the
following three appear to have been based mainly
on the authority of Shufeldt (1901:305), who
stated that
in its external narial apertures; in the possession of supraor-
bital glandular depressions; to a small degree in its lachrymal
bones; . . . in its quadrates; in the possession of large recurved
processes at the mandibular angles?the skull of the Fla-
mingo is more or less anserine in character.
The nasal region in flamingos actually differs
considerably from that of ducks, particularly in
lacking the large internal narial opening in the
rostrum characteristic of the Anseriformes.
25. "supraorbital depression": These depres-
sions accomodate salt glands and are found in a
supraorbital position in the Charadriiformes and
most other water birds, including even Hesperornis.
In the Pelecaniformes the salt glands are located
within the orbit, as they are in storks and herons,
but not in the Threskiornithidae. The condition
of this character in flamingos is as much like that
of shorebirds as that of ducks.
26. "lachrymals": In addition to Shufeldt's
comment above, Beddard (1898:441) also made
the misleading statement that the "lachrymals
are large and rather duck-like." The lachrymals
in ducks are thin, antero-posteriorly elongated
bones that are broadly fused with the skull (ex-
cept in Anseranas) and that do not nearly reach
the jugal bar. In flamingos the lachrymals are
entirely different, being unfused, thickened,
pneumatized bones that reach to the jugal bar
but have a much narrower contact with the skull.
27. "quadrate": Despite the remarks of Shu-
feldt (1901), the quadrates of flamingos are very
different from those of ducks in every aspect,
particularly in the nature of the articulation with
the lower jaw.
28. "mandibular angle": This refers to the
long, recurved, bladelike retroarticular processes
of the mandible, which are superficially very
similar in ducks and flamingos. Nevertheless there
are differences in the development of these struc-
tures between the two groups and the similarities
probably are the result of similar needs for in-
creased attachment for M. depressor mandibulae
(page 64).
29. "pectoral girdle": Evidently Shufeldt's
(1901:313) observations have been used by Sibley
et al. for this character. Sibley and Ahlquist
(1972:7) have remarked that Shufeldt "worked in
a rather haphazard fashion, simply describing
and comparing what he happened to have before
him," and it is widely recognized that his writings
on osteology and paleontology are unreliable. We
find little similarity between flamingos and ducks
in the bones of the shoulder girdle.
30. "caeca": The caeca are well-developed in
both flamingos and Anseriformes but are rudi-
mentary in Ciconiiformes. Beddard (1898:336)
states that in the Charadrii the caeca are "nearly
always large." Large caeca are also present in
other orders of birds, such as Gruiformes.
31. "tongue shape": Although flamingos and
ducks have large fleshy tongues used in filter-
feeding, the morphology and placement is en-
tirely different in the two groups, as is the struc-
ture of the bony hyoid apparatus (page 60).
"Characters Shared with Both Orders"
32. "tufted oil gland present": A tufted oil
gland occurs in the Charadriiformes and in the
majority of other orders of birds.
33. "11 primaries": This character is mis-
8 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
placed by Sibley et al. (1969) and should be listed
as shared with the Ciconiiformes (storks only).
Ducks, shorebirds, and Ciconiiformes except
storks have 10 functional primaries, whereas in
flamingos, Ciconiidae, and Podicipedidae
(grebes) there are 11 (W. D. Miller, 1924). The
extra primary in flamingos probably evolved with
a lengthening of the wing, as the number of
secondaries in flamingos is considerably greater
than in storks (page 34). The taxonomic distri-
bution of this character strongly suggests inde-
pendent derivation in all three instances.
34. "diastataxic": The diastataxic condition
of the secondaries is found in many orders of
birds, including all the Charadriiformes.
35. "carinate": An entirely useless character
in this instance, as all birds except the "ratites"
are "carinate."
36. "desmognathous": The so-called des-
mognathous condition of the palate is found in
other orders and must have evolved numerous
times from the schizognathous condition. The
fossil bird Presbyomis shows that the desmogna-
thous palate of ducks must have evolved from the
schizognathous palate of shorebirds (Olson and
Feduccia, in press) and the same is likely true of
flamingos.
37. "holorhinal": As with the preceding, the
holorhinal nostril occurs in many orders, includ-
ing certain Charadriiformes (e.g., Burhinus, Pluvi-
anus). This character varies within the Ciconi-
iformes (as presently constituted) in that the
Threskiornithidae are schizorhinal, except for
spoonbills (Platalea), which are sometimes second-
arily holorhinal, thus demonstrating the probable
ease with which the holorhinal condition can
arise.
38. "pervious nares": A condition found in
most birds, including Charadriiformes.
39. "no ectocondylar process": This refers
presumably to the ectepicondylar prominence at
the distal end of the humerus, though it is not
evident why this should have been mentioned in
any discussion of flamingos. The ectepicondylar
prominence is developed into a large spur in
Procellariiformes and most Charadriiformes but
is usually reduced in most other birds, including
flamingos. The spur, however, is absent in the
Jacanidae and Burhinidae, smaller in the Recur-
virostridae and Rostratulidae than in most Char-
adrii, and has been secondarily lost or reduced in
other Charadriiformes (e.g., Scolopax minor) and
their derivatives.
40. "16-25 cervical vertebrae": The number
of cervical vertebrae in birds may vary at almost
any taxonomic level. According to Fiirbringer
(1888, volume 2, table 41), flamingos have 18 or
19 cervicals, the Ciconiiformes have 16 or 17,
with only the Ardeidae having 18 or 19. The
Charadriiformes usually have 15, or 16 in the
case of the Burhinidae and Jacanidae. In the
Anatidae, the cervicals range in number from 16
to 25, with the high numbers occurring in the
long-necked swans. Obviously, this is a highly
adaptive character. The greater number of cer-
vical vertebrae in flamingos than in shorebirds is
probably correlated with the evolution of a long
neck associated with the exceptional feeding ap-
paratus.
41. "ambiens present": The ambiens muscle
is also present in the Charadriiformes and many
other orders of birds. In Ciconiiformes, however,
it is present only in some ibises and some storks
(Vanden Berge, 1970).
"Characters Shared with Neither Order"
42. "reduced hallux": The hallux is reduced
or absent in modern flamingos. Although thought
not to be of taxonomic consequence, the hallux is
nevertheless always present and rather well de-
veloped in the Ciconiiformes and Anseriformes.
In the Charadriiformes, on the other hand, the
hallux has been reduced or lost repeatedly. For
example, in the Recurvirostridae, the hallux is
present in Recurvirostra and absent in Himantopus
and Cladorhynchus. Sibley et al. (1969:160) note
that the short toes of flamingos are different from
either the Ciconiiformes or Anseriformes. The
toes are quite short in many Charadrii and no-
tably so in the Recurvirostridae.
43. "inverted bill": See character 44.
44. "filter apparatus": These characters are
unique to flamingos and provide one of the very
few major points of separation of the Phoenicop-
NUMBER 316
teridae from other Charadriiformes.
45. "flexor tendons type IV": Of the various
patterns of the deep flexor tendons (see George
and Berger, 1966:446-449), the Ciconiiformes and
most Charadriiformes have the type I configura-
tion, and the Anseriformes have the type II con-
figuration. Flamingos differ in having type IV
deep flexor tendons, a condition that occurs in
several groups in which the hallux is reduced or
lost, including the Recurvirostridae (page 30).
46. "1 pair syrinx muscles": A condition also
found in the Charadriiformes (including Clador-
hynchus, pers. obs.) and other orders (Beddard,
1898).
47. "small femoral-caudal [sic]": This is the
femorocaudal of Garrod (1874), designated "A"
in his thigh muscle formulae, which forms part of
the caudo-iliofemoralis of modern usage. We do
not know why Sibley et al. (1969) list this as
"small" because it is actually lacking in flamingos
(Vanden Berge, 1970), as the following character
signifies.
48. "BXY+ muscle formula": This repre-
sents only part of the expanded thigh muscle
formulae used by some modern authors (see
George and Berger, 1966:233). The formula in
most shorebirds is ABXY+, since the caudo-
femoral part of M. caudo-iliofemoralis ("A") is
usually present. This muscle is now known to be
lacking in certain genera of Charadrii (page 27),
as well as in flamingos. In storks and in herons it
is present in some genera and absent in others
(Vanden Berge, 1970), and thus appears to be
easily lost and probably of little taxonomic use.
49. "type of air cells in lung": This evidently
derives from a misreading of Weldon's (1883:639)
statement that in flamingos "the lungs present
nothing remarkable, but the air-cells and their
associated septa are strikingly characteristic."
Further reading reveals that by "air-cells" Wel-
don was referring to the air sac system (see char-
acter 14 above). Nothing in his paper indicates
that anything inside the lungs of flamingos is
distinctive.
The foregoing analysis should be sufficient to
reveal the glaring inadequacy of the anatomical
"evidence" that has been used previously in at-
tempting to determine the relationships of fla-
mingos. The characters supposedly demonstrat-
ing affinity with the Ciconiiformes we have shown
to be of wide occurrence in other orders of birds,
including the Charadriiformes, and are useful
only in showing lack of affinity with the Anseri-
formes. Advocates of a ciconiiform relationship
for flamingos are now faced with the fact that
there is not a single convincing anatomical char-
acter supportive of such a hypothesis.
Anatomical evidence for a relationship be-
tween flamingos and Anseriformes is equally de-
ficient. Some of the characters, such as webbed
feet and large caeca, are shared with the Cha-
radriiformes as well. Others, particularly feather
structure, cannot be evaluated without proper
comparison with Charadriiformes. Still other ap-
parent similarities to Anseriformes, such as the
feeding apparatus, are not really similarities at all
and are actually completely different in the two
groups. Flamingos simply possess none of the
derived characters of osteology and myology that
distinguish the well-defined monophyletic order
Anseriformes, so their ancestry must be sought
elsewhere.
Apart from features that are unique, almost
every one of the characters of flamingos cited by
Sibley et al. (1969) may be found in the Cha-
radriiformes, including all of those that do not
occur in either the Ciconiiformes or the Anseri-
formes. Thus, even without the additional infor-
mation supplied beyond, the evidence thus far
presented is much better explained by a charad-
riiform origin of flamingos.
Life History and Behavior
Various aspects of general life history and be-
havior have been summarized and discussed by
Sibley et al. (1969:163), who concluded that
many of the distinctive characteristics of flamin-
gos are probably related to their extreme gregar-
iousness, which, like the feeding apparatus, is part
of their adaptation to a "narrow ecological niche"
in "barren isolated areas." They interpreted the
10 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGV
behavioral evidence as indicating that "approxi-
mately equal numbers of behavioral elements are
shared by flamingos with the Anseriformes and
with the Ciconiiformes," and they considered it
"unlikely that any valid conclusions about rela-
tionship can be drawn from these data" (page
168). We were at first inclined to agree, but upon
reading Hamilton's (1975) accounts of behavior
in North American Recurvirostridae we were im-
pressed with the apparent similarities to flamin-
gos. This led us to the literature on the Australian
Banded Stilt, Cladorhynchus leucocephalus, where we
discovered that the life history of this species very
closely approximates that of flamingos.
Flamingos are highly social birds living in large
flocks in remote, barren areas of shallow saline
lagoons or alkaline lakes. They feed mainly on
small crustaceans and insect larvae, or in the case
of the more specialized species, on micro-
organisms such as diatoms. Because of the isola-
tion of breeding colonies, even the correct sitting
posture of incubating flamingos was not known
until 1880 (Allen, 1956); the nest and eggs of the
abundant Phoeniconaias minor were not discovered
until 1954 (Brown, 1959),xand those of Phoenico-
parrus jamesi were discovered only in 1957 (John-
son, et al., 1958). For a given flock, both the
timing and site of breeding may vary irregularly.
Nesting colonies are usually large and very
densely packed; territoriality is virtually absent,
as is response to terrestrial predators. A single,
chalky white egg, large in proportion to the bird,
is usually, but not always, deposited on a raised
cone of mud. Young are covered with white or
grayish unpatterned down and remain in the nest
for several days before departing and gathering
in large groups attended by adults, at which time
they often swim. The parents feed the young for
extended periods. This general pattern of life
history is not duplicated among any of the Cico-
niiformes or Anseriformes.
We will briefly compare the above with what
little is known of the overall life history of
Cladorhynchus leucocephalus and then compare as-
pects of the behavior of flamingos with that of
some of the better-known Recurvirostridae. Most
of the significant information relating to the life
FIGURE 1.?The 1930 nesting colony of the Australian
Banded Stilt, Cladorhynchus leucocephalus, at Lake Callabonna,
South Australia: a, part of the colony showing the extremely
close spacing of nests; b, portion of the colony with adult
birds sitting on nests; c, adults rising from nests. (Photo-
graphs from McGilp and Morgan, 1931.)
NUMBER 316 11
FIGURE 2.?The 1930 nesting colony of the Australian
Banded Stilt, Cladorhynchus leucocephalus, at Lake Callabonna,
South Australia: a, closer view of adults at nests; b, adults
with newly hatched young; c, young birds remaining in nest
after adults have temporarily departed. (Photographs from
McGilp and Morgan, 1931.)
history of Cladorhynchus may be found in the pub-
lications of Glauert and Jenkins (1931), McGilp
and Morgan (1931), Howe and Ross (1931), Jones
(1945; a summary of all previous literature on the
species), Carnaby (1946), Beruldsen (1972), Jen-
kins (1975), and Kolichis (1976). In addition, we
were fortunate to be supplied by J. A. McNamara
(1976) with a copy of his unpublished paper on
the feeding ecology of Cladorhynchus.
Cladorhynchus lives in remote areas in the south-
ern half of Australia, where it occurs in great
flocks that frequent very saline temporary lakes
in which may be found enormous quantities of
small crustaceans, upon which the birds feed
(Jones, 1945). McNamara (1976), who examined
gut contents of Cladorhynchus, found a variety of
food items, but principally brine shrimp (Parar-
temia) and brine flies (Ephydridae). In connection
with the heavy fat deposits mentioned by Sibley
et al. (1969) as being characteristic of flamingos,
it should be noted that McNamara's specimens
of Cladorhynchus had extremely heavy subcuta-
neous fat deposits, whereas specimens of Himan-
topus and Recurvirostra taken at the same time and
place did"not.
The breeding habits of Cladorhynchus remained
unknown until 1930 (Glauert and Jenkins, 1931),
a mystery not without parallel among flamingos.
It was then discovered that Cladorhynchus breeds
in great, densely packed colonies on islands and
sandbars. McGilp and Morgan (1931) estimated
nearly 27,000 pairs in a colony at Lake Calla-
bonna (Figures 1, 2). Nests consist of depressions
in the ground and are regularly spaced about 30
cm apart (Figure la). Nests in the Callabonna
colony had from 1 to 5 eggs, with most nests
having 3 eggs; clutches of 2 eggs appeared to be
complete (McGilp and Morgan, 1931; Kolichis,
1976). Adult and young birds in a colony are
practically fearless, with no apparent predator
response. The timing and place of breeding of
Cladorhynchus appear to be extremely irregular
and are correlated with variable local conditions.
For example, the great colony found on Lake
Callabonna in 1930-1931 is the only known nest-
ing record for South Australia; all others are from
Western Australia (J. A. McNamara, in litt., to
12 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
Olson, 30 May 1978).
There appears to be a nearly complete lack of
aggression or territoriality in Cladorhynchns, as is
true of flamingos. McNamara (in litt. to Olson,
30 May 1978) reports that
only once in about 110 hours observation over 8 months did
I see anything like display (courtship or otherwise). This
took place on a bank in the salt fields with dry powdery
ground; one bird knelt on the ground with wings out and
the other standing while both fenced with bills. Also at this
time one bird chased another for a short distance (10") [25
cm] then both stopped and assumed an "aggressive" posture
with head down, bill pointed at [the] other and back feathers
raised.
This could correspond to the bill-fighting and
bowing reported in Phoenicopterus by Rooth
(1965).
Furthermore, McNamara quotes Mr. Tom
Spence, Director, Perth Zoological Gardens, as
noting that
the display of the Banded Stilt is quite spectacular and very
reminiscent of that of the Lesser Flamingo. They parade in
a tight little pack with their long mantle feathers raised (just
like a Flamingo) and synchronise their movements pretty
closely. I have also seen this in the wild.
This behavior may be the exact equivalent of the
marching display of flamingos (Kahl, 1975). Rais-
ing the "back" feathers is a characteristic feature
of flamingo displays, and in the breeding plu-
mage of Cladorhynchus the tertials are greatly elon-
gated, much more so than in other Recurvirostri-
dae.
The eggs of Cladorhynchus are exceptional
among the Charadriiformes for their large size
and white ground color (Howe and Ross, 1931),
both of which recall the eggs of flamingos. Al-
though most eggs of Cladorhynchus are marked
with dark lines and blotches, as typical of other
Charadriiformes, the markings are quite variable,
and McGilp and Morgan (1931:45) reported that
a "fair proportion" were nearly immaculate and
at least one was found that was pure white (Figure
12).
Most remarkably, the young of Cladorhynchus
are clothed in white, unpatterned down (Figure 3),
a combination not met with anywhere in the
remainder of the Charadrii (Jehl, 1968), but
FIGURE 3.?Chick of the Australian Banded Stilt, Cladorhyn-
chus leucocephalus, showing the dense, unpatterned, white
down, unlike that of any other Charadrii, but similar to
flamingos.
which is typical of flamingos. A most important
point of similarity with flamingos is that Clad-
orhynchus has two coats of nestling down, a char-
acter not found in any other known shorebird
(page 34).
It is not known when the young leave the nest
or whether the adults feed the young, but McGilp
and Morgan (1931:43) report that disturbed
young "kept scampering back towards the nests"
and their photographs show many young birds
remaining in nests after the temporary departure
of adults (Figure 2c). This is in contrast to North
American Recurvirostridae as observed by Ham-
ilton (1975:89): "Even before chicks are dry, they
begin to toddle away from the nest, and soon
after the brood has hatched, the young can no
longer be found in the vicinity of the nest."
The accounts of Cladorhynchus emphasize the
rapidity of breeding and the simultaneous hatch-
NUMBER 316 13
ing of young in a colony. The young aggregate
and are attended by adults, which is probably
not different from the so-called "creche" behavior
of flamingos. McGilp and Morgan (1931) men-
tion "three old birds leading perhaps 60 young
ones into the water" and they include a photo-
graph of a flock of chicks swimming off into the
lake in the manner of young flamingos. At Lake
Marmion, Western Australia, Kolichis (1976:116)
"saw Banded Stilts on the water in small groups
varying from three young with two adults to
about 40 young with six to nine adults."
Cladorhynchus provides a nearly perfect inter-
mediate in its life history and development be-
tween flamingos and the more typical Recurvi-
rostridae and thus supplies evidence not only that
flamingos are derived from the Charadrii, but
more particularly from the Recurvirostridae.
There could hardly be a more rewarding en-
deavor for a field ornithologist than a detailed
comparative ethological study of Cladorhynchus
and flamingos.
In analyzing the ecological requirements of the
Recurvirostridae, Hamilton (1975:14) found that
although Himantopus generally resorts to fresh wa-
ter, "avocets [Recurvirostra] prefer alkaline or saline
habitats." They feed mainly upon brine shrimp,
Artemia, and adults and larvae of brine-flies, Ephy-
dra (Hamilton, 1975; Wetmore, 1925:14). We
have already noted the similar food habits of
Cladorhynchus. On Bonaire the "staple diet" of
flamingos is the larvae and chrysalids of Ephydra
(Rooth, 1965:51).
Sibley et al. (1969:164) maintained that adult
flamingos do not voluntarily swim, and inter-
preted this as being contrary to an anseriform
derivation, thereby implying similarity to Cico-
niiformes. Rooth (1965) records Phoenicopterus ruber
on Bonaire as swimming while feeding. Brown
(1975:42), in countering Sibley et al., stated that
Phoeniconaias minor in Africa feeds from near the
surface of the water away from the shoreline and
"habitually swim; in fact they could not have
reached their present numbers if they did not
swim" (see Figure 4).
While swimming, flamingos may feed by tip-
ping up in manner reminiscent of swans and
dabbling ducks, which has been interpreted as an
indication of relationship. Rooth (1965:43) de-
scribes this behavior in Phoenicopterus ruber as fol-
lows:
The head, neck and the rostral part of the body are totally
immersed, more or less straight down. The rear part of the
body then sticks up out of the water, so that the legs have to
carry out all possible movements to preserve the balance of
this position... .This unsteady position necessitates that the
movements of the feet can take place in the surface water
only. It can be seen that the tibiotarsus is directed at an
angle upwards and that only one half or three quarters of
the tarso-metatarsus is in the water.
Avocets and Cladorhynchus likewise do a consid-
erable amount of feeding while swimming and
also tip up in order to obtain food (Ross, 1924;
Hamilton, 1975; McNamara, 1976; Dinsmore,
1977). Compare the following description for Re-
curvirostra americana as given by Hamilton (1975:
52) with that of Phoenicopterus ruber above.
The feeding bird immerses its head and breast into the water
by tipping on the transverse axis from a swimming or breast-
wading position and brings the bill to the bottom. The
upended position of the bird is maintained by a backward
kick of the feet; the tibiotarsi often break the surface....
Flamingos vocalize in flight and the calls of
some are reminiscent of gooselike honkings, which
has also been cited as favoring anseriform affini-
ties. The notes of Phoeniconaias minor are higher
pitched than in Phoenicopterus ruber and have been
likened to a "yelping" (Cramp and Simmons,
1977:367). Proper comparisons are wanting, but
it should be noted that the Recurvirostridae are
notorious for vocalizing in flight and "yelping" is
a term commonly employed to describe the sound
of their nearly incessant calls when disturbed on
the breeding grounds.
The use of neck postures in the threat displays
of flamingos was likened to that in the Anatidae
by Sibley et al. (1969), whereas the raising of the
scapular and the back feathers in threats was said
to be more characteristic of the Ciconiiformes.
Both of these behavioral components are found
in the Recurvirostridae (Hamilton, 1975, fig. 15).
Bill-dipping or displacement drinking, which is
performed by flamingos and ducks but not Ci-
coniiformes (Sibley et al., 1969), is also part of the
14 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 4.?Lesser Flamingos, Phoeniconaias minor, at Lake Hannington, Kenya, showing
numbers of birds swimming in the middle of the lake. (Photograph by Alan Feduccia.)
normal precopulatory display in the Recurviros-
tridae (Hamilton, 1975:73). The near absence of
specialized pairing displays and the seasonal pair
bonds of flamingos are likewise characteristic of
the Recurvirostridae. In both flamingos and re-
curvirostrids, in such courtship as exists, there is
a similar heavy reliance on ritualized preening,
bill-dipping, head shaking and splashing of water.
The "bowing" display in Phoenicopterus (Rooth,
1965:88, fig. 14) might be equivalent to the
posture assumed in the "Group Circle" display of
Recurvirostra americana (Hamilton, 1975:68, fig.
16a). In flamingos, the "attraction function of
courtship display to other members of the species"
was cited by Sibley et al. (1969:167) as resembling
the Ciconiiformes. However, Hamilton (1975:68)
observed that the ritualized special postures used
in highly social group interactions in the Recur-
virostridae "seem to attract conspecifics from near
and far."
Copulation in flamingos takes place away from
the nest and usually in water, unlike Ciconi-
iformes but similar to most Anseriformes (Sibley
et al. 1969). The same is true, however, in the
Recurvirostridae. The reader is invited to note
the similarity in the copulatory posture of Phoen-
icopterus (Rooth, 1965; fig. 16) and that of Recur-
virostra americana (Hamilton, 1975, fig. 17*).
Although under certain circumstances flamin-
gos will lay their eggs in a depression in the
ground, as do most shorebirds, they usually con-
struct a characteristic truncated cone of mud,
upon which to deposit the egg. According to
Rooth (1965:99-100), "the function of these high
constructions is clear at high water although the
literature often reports the flooding of colonies,
NUMBER 316 15
despite the high nests." He then adds, "It is
typical that the wader Himantopus himantopus [Re-
curvirostridae] which breeds along the shores of
the salinas [on Bonaire] also makes such high
nests!" The exclamation point is his; we can only
regret in light of the present discussion that this
statement was not elaborated upon. Nests of avo-
cets and stilts usually consist of a depression in
the ground lined with any available material,
including mud chips (Hamilton, 1975:82). In a
number of references cited by Hamilton (1975:
83), avocets and stilts are reported as adding
material to their nests during floods to raise the
eggs up on a platform. All 15 nests in a colony of
Recurvirostra avosetta were adjusted in this manner
during a night of heavy rains (Makkink, 1936:
35). Certainly it is not difficult to envision that
this behavior could be modified to produce that
of flamingos, whereas the nest-building habits of
Ciconiiformes, which generally construct arboreal
platforms of sticks, does not seem at all appropri-
ate as a precursor of the phoenicopterid method.
Although none of the other Recurvirostridae
are as highly colonial as Cladorhynchus, all are
gregarious and their nesting sites are composed
of loose aggregations to which the term "colony"
is consistently applied in the literature. As with
flamingos there is no site fidelity and colonies
tend to shift location from one year to the next
(Hamilton, 1975:79).
In contrast to the Ciconiiformes, with their
elaborate nest-relief ceremonies during incuba-
tion, flamingos have almost none?one bird walks
up and its partner walks away, sometimes indulg-
ing in displacement feeding (Rooth, 1965:107).
Much the same behavior is recorded for the Re-
curvirostridae, although Hamilton (1975:85) in-
terpreted the displacement "feeding" as displace-
ment nest building, in which objects are picked
up and tossed about.
Apparently the only unique etho-ecological ad-
aptations of flamingos not found in recurviros-
trids are the parental feeding of the young (pos-
sibly present in Cladorhynchus) and the single egg
clutch. Both of these must be directly correlated
with the highly specialized feeding apparatus of
adult flamingos. Because this structure does not
develop until late in ontogeny, some parental
feeding of young would be a necessity. The single
egg clutch probably evolved as a result of this
increased parental responsibility.
The foregoing is only a brief sketch, but should
serve to illustrate the similarities in the life history
and behavior of flamingos and the Recurvirostri-
dae. Not only can all the supposed ciconiiform
and anseriform behavioral traits of flamingos be
accounted for by having flamingos derived from
the Charadrii, but also the seemingly unique
characteristics of the Phoenicopteridae that are
irreconcilable with either storks or ducks can be
explained as well.
Myology
Vanden Berge (1970) conducted a broad, com-
parative study of the appendicular myology of
the Ciconiiformes, including the Phoenicopteri-
dae. We regard it as significant that he found "no
consistent pattern in the appendicular muscula-
ture of the Ciconiiformes [that] contributes sig-
nificantly to a taxonomic clarification of this
large, loosely applied assemblage of long-legged,
long-necked, wading type birds" (page 361). Such
a conclusion would be expected if the Ciconi-
iformes were entirely an artificial group (Olson,
1979). In the following comparisons we use "Ci-
coniiformes" for the families traditionally in-
cluded in the order, but excluding flamingos.
One of Vanden Berge's most interesting discov-
eries was a previously unknown thigh muscle,
unique to flamingos, to which he later applied
the name M. iliotibialis medialis (Vanden Berge,
1976). In preliminary dissections we discovered
this muscle in Cladorhynchus, whereas it was absent
in Recurvirostra and Himantopus. This highly im-
portant discovery led us to examine the rest of the
appendicular myology of Cladorhynchus to make
further comparisons with flamingos. Details are
presented in the following section. The tabula-
tions below summarize myological comparisons
between flamingos, Cladorhynchus, and Ciconi-
iformes, especially storks. Naturally, not all of
these characters are of equal value.
16 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
A. Unique Character in Which Flamingos and
Cladorhynchus Differ from All Known Birds
1. Presence of M. iliotibialis medialis.
B. Characters Shared by Flamingos and
Cladorhynchus That Differ
from All Ciconiiformes
1. Origin of M. latissimus dorsi pars cranialis not partly
from cervical vertebrae.
2. Origin of M. latissimus dorsi pars metapatagialis partly
from synsacrum.
3. Far caudal origin of M. serratus superficialis pars cau-
dalis.
4. More distal origin of M. scapulohumeralis caudalis.
5. M. pectoralis pars subcutanea thoracica and pars sub-
cutanea abdominalis present and well-developed.
6. M. tensor propatagialis pars brevis with two separate
tendons.
7. Greater fusion of tendons of M. extensor metacarpi
radialis.
8. Distal head of M. extensor longus digiti majoris vestigial.
9. Both origin and insertion of M. adductor alulae fleshy.
10. Nature of origin of M. interosseus ventralis (particularly
different from storks).
11. Combination of M. iliofemoralis internus being short
and stout and inserting caudal to origin of M. femoro-
tibialis internus.
12. Ambiens present and inserting directly on belly of M.
flexor perforatus digiti II.
13. Nature of flexor cruris lateralis complex.
14. Greater proximal width of flexor cruris medialis.
15. None of the digital flexors with a fleshy origin from shaft
of fibula.
16. M. flexor perforans et perforatus digiti II with two heads.
17. M. flexor perforans et perforatus digit III with two
heads.
18. Insertion of M. popliteus distal to origin.
19. Deep flexor tendons type IV.
20. M. extensor hallucis absent.
21. M. flexor hallucis brevis vestigial.
C. Characters Shared by Flamingos,
Cladorhynchus, and One or More
Ciconiiformes but Differing from Storks
1. Propatagial slip of M. biceps brachii present and well-
developed.
2. M. iliofemoralis ("B") present.
3. Scapular origin of M. triceps brachii entirely fleshy.
4. Origin of M. latissimus dorsi caudalis from last free
vertebra, synsacrum, and fasciae.
5. M. scapulohumeralis cranialis present.
6. Origin of M. coracobrachialis cranialis tendinous.
7. Ventral head of M. deltoideus minor present and rea-
sonably well-developed.
8. Postacetabular portion of M. iliotibialis lateralis present.
9. Pars accessoria, M. flexor cruris lateralis, present.
10. Extensive fleshy insertion of M. pubo-ischiofemoralis.
11. More proximal origin of M. adductor digiti II.
12. Insertion of M. iliofemoralis internus caudal to origin of
M. femorotibialis internus.
D. Characters in Which Flamingos and Storks
Differ from Other Ciconiiformes
but Also Agree with Cladorhynchus
1. M. fibularis brevis absent.
2. Nature of origin of M. serratus profundus.
3. More tendinous origin of M. rhomboideus superficialis
pars scapularis.
4. M. iliofemoralis short and stout.
E. Characters in Which Cladorhynchus
Differs from Flamingos
1. M. iliotibialis medialis inserts on patellar tendon.
2. More fusion in elements of tensor propatagialis complex.
3. M. flexor hallucis brevis arises more proximally.
4. M. subcoracoideus with two distinct heads.
5. Origin of M. humerotriceps.
6. Lateral head of M. subscapularis smaller and more
dorsolaterally situated.
7. Nature of M. pectoralis propatagialis.
8. Nature of insertion of M. coracobrachialis cranialis.
9. Belly of M. ulnometacarpalis ventralis longer.
10. Total lack of fusion in the parts of M. femorotibialis.
11. Heads of M. gastrocnemius with less distal fusion.
12. M. serratus superficialis pars metapatagialis from two
distinct slips.
13. M. caudofemoralis ("A") present.
14. Belly of M. flexor digitorum profundus notched by
insertion of M. brachialis.
15. M. pronator profundus fused with M. extensor longus
digiti majoris.
16. Origin of M. fibuiaris longus not fleshy.
The appendicular myology of flamingos in no
way supports a relationship with the Ciconi-
iformes. The preceding tabulation lists 22 char-
acters in which flamingos differ from all Ciconi-
iformes and 34 in which they differ from the
Ciconiidae in particular. In all of these characters
flamingos agree with Cladorhynchus, even to the
possession of M. iliotibialis medialis, a muscle not
known to occur in any other birds.
Differences between Cladorhynchus and flamin-
gos are summarized in tabulation E. Of these,
characters 1 through 3 are but modifications of
flamingo-like conditions not found in any cico-
niiform. Characters 4 through 8, and possibly 9,
NUMBER 316 17
probably represent a single functional complex
associated with changes in pneumatization of the
humerus and consequent modification of the
shoulder. Characters 10 through 13 involve only
fusion of muscles to derive a flamingo-like state
and may be size-related. Character 13 has no
taxonomic value even at the family level. The
significance of characters 14 through 16 is not
apparent, but all of them are variable within the
Ciconiiformes, as currently constituted.
The differences between flamingos and Clado-
rhynchus are both fewer in number and less in
significance than those between flamingos and
Ciconiiformes. Appendicular myology provides
strong evidence in favor of a relationship between
flamingos and Charadriiformes, particularly
Cladorhynchus, whereas there is almost no similar-
ity between flamingos and storks.
APPENDICULAR MYOLOGY OF Cladorhynchus
We dissected the appendicular musculature in
a single adult female of Cladorhynchus leucocephalus
(SAM B30446), making comparisons chiefly with
the descriptions of ciconiiform myology in Van-
den Berge (1970). Beyond checking for the pres-
ence of M. iliotibialis medialis in various Recur-
virostridae, we have made no attempt to compare
Cladorhynchus with other shorebirds, nor have we
repeated Vanden Berge's dissections of flamingos
except to check a few specific muscles in two
rather emaciated specimens of Phoeniconaias minor,
the only fluid-preserved flamingos immediately
available to us. Vanden Berge (1970) did not
examine this species but dissected specimens of
Phoenicopterus ruber, P. chilensis, and Phoenicoparrus
jamesi. It is not our purpose to provide a detailed
description of the myology of Cladorhynchus, but
mainly to present a comparative assessment of its
similarities and differences with regard to flamin-
gos.
We have adopted the myological nomenclature
of the Nomina Anatomica Avium (Baumel et al.,
1979), using the sequence of Vanden Berge's
(1970) original paper for facility of comparison
and quoting his nomenclature in parentheses
when it differs substantially from that of the NAA.
For certain muscles, Vanden Berge (1970)
found little or no significant variation within the
Ciconiiformes. Of these, those in Cladorhynchus
that did not differ from his descriptions are listed
as follows and are not discussed further: M.
brachialis, M. supinator, M. flexor digitorum su-
perficialis ("sublimus"), M. extensor digitorum
communis, M. extensor metacarpi ulnaris, M.
ectepicondylo-ulnaris ("anconeus"), M. flexor al-
ulae ("flexor pollicis"), M. extensor brevis alulae
("extensor pollicis brevis"), M. abductor digiti
majoris ("abductor indicis"), M. iliotrochanteri-
cus cranialis, M. iliotrochantericus medius, M.
iliofibularis ("biceps femoris"), M. tibialis crani-
alis, M. extensor digitorum longus, M. plantaris.
M. latissimus dorsi pars cranialis
{"anterior")
This is a broad, very thin muscle arising as a
thin tendinous sheet from the spinous processes
of the second through fourth thoracic vertebrae.
The insertion is fleshy on the cranial surface of
the proximal third of the humerus.
Vanden Berge (1970) found that this muscle in
flamingos originated from the first through third
thoracics, whereas in all other Ciconiiformes the
origin involved one or more cervical vertebrae.
Despite the fact that in one skeleton of Cladorhyn-
chus we examined, the first thoracic rib had no
sternal component and would therefore have to
be considered as a "cervical," our evidence sug-
gests that the origin of M. latissimus dorsi crani-
alis is from the same series of vertebrae as in
flamingos. In neither flamingos nor Cladorhynchus
is the origin in part from the true cervical series
as it is in Ciconiiformes.
M. latissimus dorsi pars caudalis
^posterior'")
The origin is tendinous mainly from the cranial
margin of the ilium and also from the last free
vertebra and surrounding fasciae. This is as de-
scribed by Vanden Berge (1970) for flamingos
and ibises and differs from that of herons (dorsal
vertebrae only), Balaeniceps (last 2-3 free verte-
brae and synsacrum) and storks (origin not in-
volving fasciae).
18 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
M. latissimus dor si pars metapatagialis
This slender but well-developed muscle origi-
nates from the cranial tip of the synsacrum and
partly from the last free thoracic vertebra. The
insertion subtends the humeral feather tract. Fla-
mingos agree with Cladorhynchus in having the
origin partly from the synsacrum whereas in the
Ciconiiformes it is entirely from the vertebrae.
M. rhomboideus superficialis
PARS CLAVICULARIS.?The origin is a thin ten-
dinous sheet from the last cervical and first tho-
racic vertebrae and the insertion is fleshy along
the cranial portion of the dorsal (vertebral) mar-
gin of the scapula extending ventrad on the ad-
jacent dorsal projection of the clavicle, ventral to
the origin of M. tensor propatagialis.
PARS SCAPULARIS.?The origin is a tendinous
sheet extending from the second thoracic vertebra
to the last free thoracic. The insertion is fleshy on
the dorso-medial margin of the cranial three-
fourths of the scapular blade, extending as far
caudally as the bend in the blade.
According to Vanden Berge (1970) a more
extensively tendinous pars scapularis differen-
tiates flamingos and storks from other Ciconi-
iformes; Cladorhynchus fits this pattern, though the
origin is longer than reported for those forms.
M. rhomboideus profundus
This deep muscle arises as a broad, thin, ten-
dinous sheet from the spinal processes of the first
through the fourth thoracic vertebrae. The inser-
tion is fleshy along the costal aspect of the caudal
four-fifths of the scapula. This condition agrees
generally with that of most Ciconiiformes except
Balaeniceps (Vanden Berge, 1970).
M. serratus profundus
This muscle consists of three distinct slips aris-
ing fleshy from the last cervical and first two
thoracic ribs; these insert fleshy on the costal
surface of the cranial half of the scapula.
Flamingos and storks both agree with the con-
formation in Cladorhynchus. These differ, on the
one hand from herons, in which the muscle arises
only from cervical vertebrae (four fleshy slips) or
from cervical vertebrae and the first thoracic (five
slips), and on the other hand from ibises and
Balaeniceps, in which the three slips arise from the
last two cervical and first thoracic vertebrae.
M. serratus superficialis pars cranialis
and pars caudahs
These are entirely separate muscles in Clador-
hynchus. Pars cranialis arises fleshy from the last
cervical and first thoracic ribs, with a thin ten-
dinous sheet spreading to the penultimate cervi-
cal. The insertion is by a thin tendinous sheet
attaching to the cranial sixth of the ventral mar-
gin of the scapula. Pars caudalis originates from
a thin sheet of tendon on the third through sixth
thoracic ribs and inserts by a thin tendinous sheet
on the ventral margin of the caudal third of the
scapula. In the far caudal origin of M. serratus
superficialis caudalis, flamingos differ from Ci-
coniiformes and agree with Cladorhynchus. In his
one specimen of Phoenicopterus chilensis, Vanden
Berge (1970:303) found the origin to be on tho-
racics 2 through 4, as in storks and some ibises.
Phoenicoparrus jamesi and Phoenicopterus ruber were
shown to be unique in the Ciconiiformes in hav-
ing the origin from thoracics 2 through 5, and in
the latter species "the origin extended posteriorly
almost to the sixth thoracic," the condition met
with in Cladorhynchus.
M. serratus superficialis
pars metapatagialis
This well-developed muscle consists of two dis-
tinct slips, one arising fleshy from thoracic ribs 4
and 5 and the other arising tendinously from the
sixth thoracic. The insertion is on the humeral
feather tract?we did not notice that it fused with
M. latissimus dorsi metapatagialis or that there
was a tendinous slip to the scapula as described
for flamingos and herons (Vanden Berge, 1970),
but either condition may have been obscured by
specimen damage.
Cladorhynchus appears to differ from flamingos
in that separate slips are not mentioned by Van-
den Berge (1970). The more caudal origin in
Cladorhynchus agrees with Phoenicopterus ruber but
the origin in P. chilensis and Phoenicoparrus is re-
NUMBER 316 19
ported to be from thoracics 3 to 5 as in storks and
ibises (Vanden Berge, 1970).
M. scapulohumeralis cranialis
This is a very small, entirely fleshy muscle, only
a few fibers wide. The origin is from the ventral
surface of the glenoid facet of the scapula; at its
midpoint it is partly attached to M. scapulohu-
meralis caudalis. The insertion is just distal to the
ridge dividing the tricipital fossa, between the
humeral heads of M. triceps brachii.
Vanden Berge (1970) found this muscle only
in herons and two species of flamingos, but not in
Phoenicopterus ruber or any other Ciconiiformes. It
was well-developed in the fossil flamingos Palae-
lodus and Juncitarsus and its reduction or loss in
modern species may be correlated with increased
pneumatization of the humerus and the conse-
quent loss of area for insertion.
M. scapulohumeralis caudalis
The origin is fleshy from the full length of the
dorsal and lateral surfaces of the scapula except
for that part occupied by M. subscapularis caput
laterale ("pars externa"). The insertion is both
tendinous and fleshy on the distal end of the
ventral rim of the tricipital fossa. The more pos-
terior origin is apparently similar to that of fla-
mingos and differs from herons and storks (Van-
den Berge, 1970).
M. pectoralis
The origins of this great muscle are both fleshy
and tendinous from the postero-lateral process of
the sternum and adjacent ribs, fleshy from the
ventral rim of the carina and from the lateral
surface of the clavicle and Membrana sternocor-
acoclavicularis. The insertion is partly by a ten-
dinous connection to the bicipital surface of the
humerus but with the principal tendon attaching
on the ventral margin of the deltoid crest. M.
pectoralis is partially divided into two distinct
layers; a larger external one with a tendinous
sheet on its antero-medial surface separating it
from a smaller medial muscle layer. These layers
fuse only in the posterior fourth of the whole
muscle mass.
As discussed previously, much was made in the
earlier literature of the layering of this muscle in
flamingos, but as we have seen, this serves only to
separate them from ducks and will not distinguish
them from a variety of other birds, including
shorebirds such as Cladorhynchus.
M. pectoralis pars propatagialis
This subcutaneous slip of the pectoralis is only
weakly differentiated in Cladorhynchus, being rep-
resented by the separation of fibers attaching
along a raphe that also forms the origin of M.
tensor propatagialis. Vanden Berge (1970) indi-
cates this muscle to be best developed in herons
and flamingos within the Ciconiiformes, but such
would not appear to be the case in Cladorhynchus.
M. pectoralis pars subcutanea thoracica
and abdominalis
Pars subcutanea thoracica and Pars subcuta-
nea abdominalis are present and constitute a
broad, well-developed sheet on the skin of the
breast and flank, attaching to the lateral abdom-
inal wall and to the pubis. Vanden Berge (1970)
found both slips to be well-developed in flamin-
gos. In herons, pars subcutanea abdominalis is
present or absent; pars subcutanea thoracica is
present but very narrow. Both slips are absent in
storks, ibises, and Balaeniceps. Thus, flamingos
agree much better with Cladorhynchus in this re-
spect than with any Ciconiiformes.
M. supracoracoideus
The origin is fleshy from the dorsolateral sur-
face of the carina and the medial portion of the
body of the sternum; although the belly lies over
the sternocoracoclavicular membrane, it does not
seem to attach to it. The muscle tapers to a
tendon that passes through the triosseal canal to
insert dorsally on the dorsal tubercle ("external
tuberosity") of the humerus. Vanden Berge
(1970) does not specifically mention the condition
of this muscle in flamingos.
M. coracobrachialis cranialis
This is very well developed in Cladorhynchus,
arising tendinously from the lateral surface of the
20 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
head of the coracoid and the glenoid joint cap-
sule. The insertion is very strong both by tendons
in the ligamental furrow and to the prominence
between the ligamental furrow and the bicipital
furrow (impressio m. coracobrachialis cranialis)
and by fleshy fibers on most of the bicipital
surface. Distally it forms a sheet of tendon that is
continuous with the origin of the dorsal (cora-
coidal) head of M. biceps brachii. The tendinous
origin agrees with flamingos, herons, and Balaen-
iceps and differs from storks and ibises, but the
insertion in Cladorhynchus is quite different from
that described for flamingos or any of the Cicon-
iiformes by Vanden Berge (1970), and is probably
typical for the Charadriiformes, to judge by the
conformation of their humeri.
M. coracobrachialis caudalis
The origin is fleshy from the lateral process of
the sternal end of the coracoid and the adjacent
portion of the sternum, with a tendinous connec-
tion to the tip of the craniolateral (sternocora-
coidal) process of the sternum. The insertion is by
a tendon to the tip of the ventral tubercle ("in-
ternal tuberosity") of the humerus. The origin
partly from the sternum agrees with flamingos,
two species of herons, and two genera each of
storks and ibises studied by Vanden Berge (1970),
whereas in all other forms the origin was found
to be confined to the coracoid.
M. sternocoracoideus
The origin is mixed fleshy and tendinous from
the ventral surface of the craniolateral process of
the sternum and the first two sternal ribs. The
insertion is fleshy in the sternocoracoidal impres-
sion and process of the coracoid. We did not
detect any layering in this muscle as described by
Vanden Berge (1970) for flamingos and storks.
M. subcoracoideus
This is a large, bulging, rounded muscle mass
with two distinct heads. The dorsal head arises
fleshy from the medial surface of the dorsal part
of the clavicle, while the larger ventral head arises
fleshy entirely from the medial surface of the
sternocoracoclavicular membrane. These heads
become extensively commingled with M. sub-
scapularis and contribute to a common tendinous
insertion with that muscle.
M. subcoracoideus is weakly developed in her-
ons and Balaeniceps and is more extensive in other
Ciconiiformes and flamingos. Cladorhynchus differs
from all of them in having two separate heads, a
condition that is typical of many other birds,
however (George and Berger, 1966).
M. subscapularis
This muscle arises from two distinct heads lying
on opposite sides of the scapula. The lateral (ex-
ternal) head originates fleshy from the dorsolat-
eral surface of the cranial fifth of the scapula,
behind the glenoid. The medial (internal) head
originates fleshy from most of the costal or ventral
surface of the scapula, with a long, narrow, ta-
pering extension running the full length of the
ventral margin. The insertion is a common ten-
don with M. subcoracoideus on the ventral tu-
bercle of the humerus. In the clearly dorso-lateral
position and short length of the lateral head,
Cladorhynchus differs from the condition described
for flamingos and the Ciconiiformes, in all of
which except herons the external head is de-
scribed as being as large as, or larger than, the
internal head (Vanden Berge, 1970).
M. tensor propatagialis
Pars longa has a partly fleshy attachment on
the proximal end of the deltoid crest and a broad
tendinous attachment to the propatagial slip from
M. pectoralis. In addition, the belly extends prox-
imally over the shoulder and has a common origin
with pars brevis from the dorsal portion of the
clavicle.
Par brevis terminates as two separate tendons
(Figure 5a), the proximal tendon inserting di-
rectly on dense fasciae over the tendon of origin
of M. extensor metacarpi radialis. The distal
tendon is closely bound to that of pars longa
proximally; at the level of the propatagial elastic
ligament, it diverges to insert on the proximal
forearm as a bifurcated tendon. The distal ramus
of this bifurcation is wider and receives an inelas-
tic tendinous slip from the elastic ligament itself.
NUMBER 316 21
The elastic ligament of the propatagium is
directly continuous with the tendon of pars longa
and, at the same level, receives the propatagial
slip from M. biceps brachii. The elastic ligament
then trifurcates in a complicated manner, the
three rami merging distally to form a distal in-
elastic tendon that is buried in a sheath in the
leading edge of the propatagium. This inelastic
tendon encloses a tough fibrous dilation imbed-
ded in the skin opposite the insertion on the
carpal joint. In addition to the inelastic tendinous
slip that unites with the bifurcated tendon of pars
brevis, previously mentioned, there is also a very
narrow tendon from the leading elastic ramus; it
terminates on the retinaculum that restrains the
tendon of the superficial digital flexor.
Vanden Berge (1970) reports that flamingos
differ from all Ciconiiformes in possessing two
separate tendons of pars brevis. This, in fact,
appears to be a feature characteristic of Charad-
riiformes, as Fiirbringer (1902, pi. 21: figs. 218?
219) illustrates a similar condition in Larus (Lar-
idae) and Parra (? Jacana, Jacanidae). In the
specimen of Phoeniconaias we examined (Figure
5b), M. tensor propatagialis was similar to that of
Cladorhynchus except that there was no fusion of
the distal tendon of pars brevis with the tendon
of pars longa proximally; the smaller propatagial
slip of the biceps, instead of fusing to this com-
bined tendon gives rise to a small, partially elastic,
separate tendon that inserts far distally on the
tendon of pars longa, near the distal end of
the radius. Most of the differences exhibited by
Cladorhynchus could probably be accounted for by
fusion of elements present in flamingos. M. tensor
propatagialis in flamingos and Cladorhynchus is
very different from that of storks (see Fiirbringer,
1902, pi. 21: fig. 222).
M. deltoideus major
This arises fleshy from the dorsal portion of the
scapula between the acromion and the glenoid
biceps brachii __
propatagial slip
biceps brachii
propatagial slip
tensor propatagialis
pars brevis
tensor
propatagialis
pars brevis
FIGURE 5.?Dorsal view of right wing to show configuration of M. tensor propatagialis in
Cladorhynchus leucocephalus (a) and Phoeniconaias minor (b). The double tendon of pars brevis
appears to be a fairly typical charadriiform character that is absent in storks. The biceps slip is
also typical of Charadriiformes and occurs in "Ciconiiformes" only in the Threskiornithidae.
Blackened portions indicate elastic tendons. (Not to scale.)
22 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
facet and also from the strong coraco-scapular
ligament. The belly lies on the dorsal surface of
the deltoid crest and has a fleshy attachment on
the edge of the crest and along a line tapering
distally on the shaft for one-third the length of
the humerus, becoming tendinous towards the
distal end.
The fleshy origin of this muscle is as described
for flamingos, Ciconia, Eudocimus, and Plegadis and
differs from other genera of Ciconiiformes, in
which the origin may be partly tendinous or more
lateral (Vanden Berge, 1970).
M. deltoideus minor
This muscle consists of two distinct heads orig-
inating in the triosseal canal and passing out over
the insertion of M. supracoracoideus. They are
entirely separate, at least after emerging from the
triosseal canal, with the larger dorsal head com-
pletely overlying the ventral head. The dorsal
head originates fleshy, partly from the acromion
of the scapula but mostly from the procoracoid
process of the coracoid. The insertion is fleshy on
the proximal end of the deltoid crest just distal to
the dorsal tubercle. The origin of the ventral head
was not traced, having come away with the re-
moval of M. supracoracoideus. The belly becomes
tendinous at the level of the dorsal tubercle of the
humerus and inserts in tissue in the ligamental
furrow on the ventral side of the humerus. The
ventral head is either very weak or absent in
storks and Balaeniceps, better developed in flamin-
gos, ibises, and certain herons, and best developed
in other herons (Vanden Berge, 1970); flamingos
thus agree with Cladorhynchus and differ from
storks in this respect.
M. triceps brachii
The scapular head (M. scapulotriceps) arises
both fleshy and tendinous from the lateral side of
the scapula just caudal to the glenoid facet, and
also by a short adjacent retinaculum to the edge
of the scapula slightly more caudally. There is a
tendinous retinaculum to the humerus in com-
mon with the insertion of M. latissimus dorsi pars
caudalis. The belly continues along the entire
shaft of the humerus to insert on the proximal
end of the ulna.
The humeral head (M. humerotriceps) arises
fleshy from two portions bisected by the insertion
of M. scapulohumeralis caudalis. These two por-
tions fuse on a median raphe and have fleshy
origins from the entire caudal surface of the shaft
of the humerus, occupying the double, non-pneu-
matic fossa characteristic of most Charadrii and
differing from all Ciconiiformes and flamingos.
The common tendon of these two parts inserts
both fleshy and tendinous on the olecranon.
Flamingos agree with Cladorhynchus and ibises,
except Ajaia, in having the scapular origin en-
tirely fleshy, whereas in other Ciconiiformes it is
at least partly tendinous and in storks there are
two distinct tendons of origin (Vanden Berge,
1970).
M. biceps brachii
This muscle arises from two heads; the more
ventral humeral head originates by a short tendon
from the ventro-distal edge of the bicipital crest.
The smaller dorsal or coracoidal head arises from
the broad, strong, distal tendon of M. coraco-
brachialis cranialis. This head gives rise to the
strong slip to M. tensor propatagialis. The two
heads give rise to entirely separate tendons, the
more ventral one inserting on the proximal end
of the radius, and the dorsal one inserting at the
proximal end of the "brachialis" scar of the ulna.
In the Ciconiiformes, the biceps slip is well-
developed only in flamingos and ibises. It is ves-
tigial in herons and absent in storks and Balaeni-
ceps. In the more distinct division of the belly of
the biceps, Cladorhynchus appears to differ some-
what from the forms described by Vanden Berge
(1970), in all of which the belly is essentially
undivided proximally.
M. expansor secundanorum
This is a small, diffuse muscle inserting on the
bases of 3 or 4 secondaries at the proximal end of
the ulna and from fasciae over the dorsal surface
of the elbow joint. The very slender tendon ex-
tends proximad and enters the axilla. We did not
trace the delicate origins, but encountered one of
them that emerged from connective tissue in the
NUMBER 316 23
axilla and attached to the dorsal surface of the
sternocoracoidal ligament. The belly is not
weakly developed as in herons and is therefore in
agreement with flamingos, storks, and ibises.
M. pronator superficialis
The origin is both tendinous and fleshy from
the cranioventral corner of the distal end of the
humerus ("attachment of anterior articular liga-
ment" of Howard, 1929). The insertion is by a
tendinous sheet opposite the insertion of M. su-
pinator on the cranioventral edge of the proximal
third of the radius. There is an indication of a
division in the belly. The origin is apparently
entirely tendinous in flamingos and Ciconiiformes
except Eudocimus and Ajaia (Vanden Berge, 1970).
M. pronator profundus
This arises tendinously from the ventral epicon-
dyle (entepicondyle) of the humerus and inserts
fleshy along the ventral surface of the proximal
half of the radius, including the proximal sixth or
so. It fuses distally with M. extensor longus digiti
majoris ("extensor indicis longus"). This is like
the condition described for ibises and most herons
and differs from flamingos, storks and Balaeniceps
in which the muscle becomes tendinous distally
and does not fuse with M. extensor longus digiti
majoris (Vanden Berge, 1970).
M. flexor carpi ulnaris
This is the most caudal of the ventral muscles
of the ulna and arises as a strong tendon from the
flexor process at the distal end of the humerus.
There is a proximal division of the belly, the
combined fibers of which run the full length of
the ulna. The insertion is tendinous on the ulnare.
Vanden Berge (1970) does not mention any dis-
tinctive condition in this muscle in flamingos.
M. flexor digitorum profundus
The origin is from two slips on the ventral
surface of the proximal end of the ulna that are
separated by the insertion of M. brachialis. The
tendon forms about midway along the ulna, runs
over the pisiform process, under M. flexor alulae,
and extends along the cranial edge of the carpo-
metacarpus to insert at the base of the distal
phalanx of the major digit. The belly is also
notched by M. brachialis in ibises, herons, and
Balaeniceps but evidently not in flamingos and
storks (Vanden Berge, 1970).
M. ulnometacarpalis ventralis
This differs from flamingos and Ciconiiformes
in that the belly is longer, tapering over the distal
three-fourths of the ulna.
M. extensor metacarpi radialis
This muscle is clearly divided into two bellies,
the larger ventral one arising fleshy from the
ectepicondylar spur of the humerus and the dorsal
one from a superficial tendon in common with
the insertions of M. tensor propatagialis brevis.
About three-fourths distally the length of the
radius they form a common tendon that runs
along the leading edge of the wing through a
groove in the radius, over the carpal joint, to
insert on the extensor process of the alular meta-
carpal, there partly fusing with the underlying
tendon of M. extensor longus alulae ("pollicis
longus").-
In flamingos the two bellies fuse distally and
produce a common tendon, whereas in all Cicon-
iiformes the bellies are separate and the tendons
do not fuse except at the distal end of the radius.
Cladorhynchus approaches the condition in fla-
mingos in that the fusion of the tendons is farther
proximad, although the bellies are nevertheless
completely separate.
M. extensor longus alulae
("pollicis longus")
This is about as described for flamingos and
Ciconiiformes except that we could not detect
that there were two heads as reported by Vanden
Berge (1970).
M. extensor longus digiti majoris
("indicus longus")
This muscle is as described for flamingos by
Vanden Berge (1970). The distal head is ex-
tremely small, only about 3 to 4 mm long and
less than 1 mm in width. It is better developed in
24 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
Ciconiiformes but in flamingos it occurs only as
a few fleshy fibers in Phoenicopterus chilensis and it
is absent in P. ruber and Phoenicoparrus jamesi (Van-
den Berge, 1970).
M. ulnometacarpalis dorsahs
This muscle appears to be similar to the typical
form in flamingos and Ciconiiformes in general;
there are two bellies, in contrast to the single belly
reported for Leptoptilos (Vanden Berge, 1970).
M. abductor alulae ("pollicis")
There is no suggestion of a division as reported
for Phoenicopterus ruber but not other flamingos
(Vanden Berge, 1970).
M. adductor alulae ("pollicis")
Both the origin and the insertion are fleshy; the
insertion is on the alular bone and not on feathers.
The same is true for flamingos, whereas in all
Ciconiiformes except Balaeniceps the origin is ten-
dinous distally and the insertion is mainly on
feathers, except in ibises.
M. interosseus dorsalis
The origin is as described for Ciconiiformes.
The tendon bifurcates after the metacarpopha-
langeal joint and sends a short tendon to the
dorsal surface on the proximal half of the proxi-
mal phalanx of the major digit. The other ramus
continues distally and inserts as a broad band on
the proximo-dorsal edge of the distal phalanx,
with a weaker extension going out to the tip of
the phalanx and the bases of the distal primaries.
No ramus to the proximal phalanx is mentioned
by Vanden Berge (1970) for the Ciconiiformes or
flamingos.
M. interosseus ventralis ("volaris")
The origin within the metacarpal space is from
the entire margin of the major metacarpal ("II")
and all but the distal fifth of the minor metacar-
pal ("III"). This is as in flamingos and Balaeniceps
except that in those forms the attachment to the
minor is less extensive and is confined to the
proximal half of the bone. In storks there is no
attachment to the minor, whereas in herons and
ibises the origin runs the entire length of the
minor metacarpal.
M. flexor digiti minons ("///")
The origin is fleshy, begins at the insertion of
M. ulnometacarpalis dorsalis, and extends along
the remainder of the caudal margin of the minor
metacarpal ("III"), with the longest fibers arising
in the distal third of the belly. This is in agree-
ment with flamingos, storks, and Balaeniceps,
whereas in herons and ibises the main fleshy fibers
are more proximally situated.
M. iliotrochantericus caudalis
This muscle originates fleshy from almost the
entire preacetabular ilium, the origin being some-
what more aponeurotic posteriorly. The insertion
is a broad tendon along the craniolateral surface
of the trochanter, extending proximally deep to
M. iliofemoralis externus ("glutaeus medius et
minimus"). Vanden Berge (1970) notes that in
the stork Leptoptilos this muscle is covered only by
the very extensive aponeurosis of M. iliotibialis
lateralis, whereas in the Phoeonicopteridae, as in
Cladorhynchus, it is covered by the fleshy bellies of
the iliotibialis complex.
M. iliofemoralis externus
("glutaeus medius et minimus")
The origin is fleshy from the edge of the ilium
above the acetabulum, becoming aponeurotic
caudally. The insertion is by a fairly long tendon
attaching in the middle of the lateral aspect of
the proximal end of the femur. As in the Phoen-
icopteridae, Ciconiidae, and Threskiornithidae,
the insertion is cranial to that of M. ischiofemor-
alis, in contrast to Balaeniceps and the Ardeidae,
in which it is caudal (Vanden Berge, 1970).
M. iliofemoralis internus ("iliacus")
This is a short, diagonal muscle originating
fleshy from the ventral border of the preaceta-
bular ilium and inserting fleshy on the medial
surface of the femur, below the head, proximal
and caudal to the origin of M. femorotibialis
internus. The insertion is in agreement with both
flamingos and ibises and differs from storks, in
NUMBER 316 25
which the insertion is cranial to the origin of M.
femorotibialis internus (Vanden Berge, 1970).
Cladorhynchus agrees with both flamingos and
storks in that this muscle is short and stout,
whereas in other Ciconiiformes it is long and
narrow.
M. ambiens
The ambiens is present in Cladorhynchus and
arises from a fairly long tendon from the pectineal
process of the pelvis. Its long, thin tendon of
inertion runs through the patellar tendon and
then deep to the insertion of M. iliofibularis to
insert mainly on the belly of M. flexor perforatus
digiti II, but also with a tenuous extension to M.
flexor perforatus digiti III. The ambiens is absent
in herons and Balaeniceps, and possibly in Scopus
and some storks (see references cited by Vanden
Berge, 1970:333). In those Ciconiiformes in which
the ambiens is present, the insertion "is directly
continuous with a small medial head" of M.
flexor perforatus digiti II, except in flamingos, in
which the insertion is on the belly of that muscle
(Vanden Berge, 1970:333). In this respect then,
flamingos are more similar to Cladorhynchus than
to any of the Ciconiiformes.
M. iliotibialis lateralis
This is a broad, thin sheet originating as an
aponeurosis from the dorsal crest of the ilium and
cranially from the dorsal crest of the synsacrum.
It covers much of the lateral surface of the thigh,
including a portion of M. iliofibularis ("biceps
femoris") caudally and Mm. iliotrochanterici cra-
nially. The postacetabular and preacetabular
portions are continuous and not separated prox-
imally by a tendinous sheet as in flamingos, but
distally they are separated by an aponeurosis
(Figure 6b) that fuses with the underlying M.
femorotibialis and inserts on the patellar tendon.
Flamingos differ from Cladorhynchus in having the
two heads of this muscle "separated by a thin
tendinous sheet covering the II. troc. post,
[caud.]" (Vanden Berge, 1970:335), but they are
more similar to Cladorhynchus than to the Ciconi-
idae or Scopus, in which the postacetabular por-
tion is absent and M. iliofibularis is exposed.
M. iliotibialis medialis and
M. iliotibialis cranialis ("sartorius")
In Cladorhynchus these two muscles (Figure 6b)
originate from a common aponeurosis on the
most cranial portion of the dorsal crest of the
synsacrum. M. iliotibialis medialis is a broad
(8.5 mm), thin strap underlying the M. iliotibialis
cranialis, which is considerably narrower (4.5 mm
at midpoint). The caudal portion of M. iliotibialis
medialis is covered by M. iliotibialis lateralis.
Both Mm. iliotibialis medialis and cranialis insert
on the patellar tendon, the former being more
medial to the latter. Vanden Berge (1976) reports
that M. iliotibialis medialis inserts at the base of
the inner cnemial crest of the tibiotarsus in fla-
mingos; thus in Cladorhynchus the insertion on the
patellar tendon probably represents a slightly
more primitive state. M. iliotibialis medialis was
present and developed to the same degree on both
sides of the specimen of Cladorhynchus dissected in
this study.
We examined specimens of Recurvirostra ameri-
cana (Figura 6a) and Himantopus mexicanus, in nei-
ther of which was M. iliotibialis medialis present.
The occurrence of this muscle in Cladorhynchus
and flamingos and no other known birds, is very
strong evidence of relationship. In view of the
amount of concurring data, it seems incontro-
vertible.
M. femorotibialis
M. FEMOROTIBIALIS INTERNUS.?This is a sepa-
rate muscle originating fleshy along the entire
medial face of the femur distal to the insertion of
M. iliofemoralis internus ("iliacus"). It inserts
partly by a strong tendon on the medial side of
the tibial head just behind the inner cnemial crest
and contributes weakly to the medial portion of
the patellar tendon, covering much of the medial
surface of the distal end of the femur. This tendon
does not cover the tendon of insertion of M.
iliotibialis medialis as reported for Phoenicopterus
(Vanden Berge, 1970).
M. FEMOROTIBIALIS MEDIUS.?The origin is
fleshy from the caudolateral surface of the shaft
of the femur, beginning at the level of the tro-
26 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
illotrochanterlcus
cranialis/
iliotrochintericus
caudaHs
iliafcmoralis
?xttrnus
ilietrochantericui
ialii
iliofemoralis
externus
ftmorotlbialit
fcmorotibialit
FIGURE 6. Lateral view of right th igh of Recurvirostra americana (a) and Cladorhynchtis leucocepha-
lus (b) with M. iliotibialis Iateralis reflected from origin. M. iliotibialis medialis is absent in
Recurvirostra but present in Cladorhynchtis. This muscle occurs elsewhere only in flamingos.
chanter. It barely overlaps the insertion of M.
iliotrochantericus cranialis and continues on
around to the cranial surface of the shaft at the
level of the distal extent of the trochanter. The
insertion forms much of the patellar tendon,
which, as mentioned, is partly fused with the
superficial aponeurosis of M. iliotibialis Iateralis.
M. FEMOROTIBIALIS EXTERNUS.?This is also an
entirely separate entity, not fusing with femoro-
tibialis medius. It arises fleshy from the caudola-
teral distal three-fifths of the femur. It overlies
the iliofibular ("biceps") loop and inserts as a
fairly broad tendon on the patellar tendon, distal
to most of the insertion of femorotibialis medius.
Cladorhynchus differs from flamingos, storks, and
Balaeniceps in the lack of fusion of Mm. femoro-
tibialis medius and externus. In the Ciconiiformes
the external muscle was reported as most clearly
developed in herons and ibises.
M. caudo-iliofemoralis {"piriformis")
M. ILIOFEMORALIS.?This muscle arises mainly
fleshy (tendinous caudally) from the ventral edge
of the postero-lateral corner of the ilium and
extends as a thin triangular sheet, encompassing
a small tendinous area in the middle of the dorsal
edge, to insert via a short tendon (fusing with
that of M. caudofemoralis) on the caudolateral
face of the shaft of the femur about one-third the
way distally.
M. CAUDOFEMORALIS.?This is present in
Cladorhynchus and arises from a long, thin tendon
on the ventral surface of the caudal bulb and
extends as a narrow strap across the thigh deep
to M. flexor cruris Iateralis and dorsal to M. flexor
cruris medialis, having a common insertion with
M. iliofemoralis by a fairly long tendon.
These are two of the "Garrod formula" thigh
muscles that have figured so prominently in much
of the past taxonomic literature. M. caudofemor-
alis ("A" of Garrod, 1874) is absent in flamingos
(including Phoeniconaias, this study) but is present
in Cladorhynchus. The same variation occurs within
the Ciconiidae and the Ardeidae, in which this
muscle is present in some genera but absent in
others (Vanden Berge, 1970). Fisher and Good-
man (1955) found M. caudofemoralis in two spec-
imens of Grus americana but it was absent in a
NUMBER 316 27
third. Within the Charadriiformes it has been
reported as absent in Burhinus (George and Berger,
1966). The late George Hudson (unpublished
MS, fide Vanden Berge) found it to be present in
Burhinus bistriatus, however, but absent in several
genera of Scolopacidae and in Steganopus and
Lobipes (Phalaropodidae).
M. iliofemoralis ("B" of Garrod) is present in
Cladorhynchus, flamingos, and ibises, but is uni-
formly absent in other Ciconiiformes.
M. flexor cruris lateralis
("semitendinosus")
Both parts of the muscle present somewhat of
an anomalous condition in Cladorhynchus (Figure
la). Pars pelvica arises from a broad aponeurosis
on the caudo-lateral corner of the ilium, being
partly fused with the aponeurosis of origin of M.
transversus cloacae. It passes distally as a narrow
strap to insert on a very short, nearly vertical
raphe shared with pars accessoria, the fibers of
which fuse with the slender belly of M. gastro-
cnemius pars intermedia to insert fleshy in the
popliteal fossa of the femur, some of the fibers
fusing medially with M. pubo-ischiofemoralis
pars lateralis. There is no medial tendon from the
raphe to the underlying M. flexor cruris medialis.
Vanden Berge (1970:338) states that in herons,
Balaeniceps, and flamingos pars accessoria is
clearly separable from M. gastrocnemius pars
intermedia and that in the Phoenicopteridae "the
fleshy insertion extends over the distal three-fifths
of the femoral shaft." He did not examine Phoen-
iconaias, however, and the two specimens we dis-
sected differed greatly from his description for the
other genera of flamingos. In lateral view (Figure
1b), the arrangement in Phoeniconaias is quite sim-
ilar to that seen in Cladorhynchus except that the
raphe between pars pelvica and pars accessoria
extends as a long diagonal intersection that is
continuous with M. gastrocnemius pars interme-
dia. Therefore, pars accessoria in Phoeniconaias is
not separable and attaches to a shorter area on
the distal end of the femur, far less than three-
fifths of the femoral shaft. In medial view (Figure
8) the raphe is more distinct and gives off a
tendinous slip to the tendon of insertion of M.
flexor cruris medialis, unlike Cladorhynchus.
In most birds possessing both parts of the lat-
eral flexor, the fibers meet at a greater angle than
in Cladorhynchus and Phoeniconaias. It is difficult to
reconcile what we observed in Phoeniconaias with
Vanden- Berge's description of flamingos based
on Phoenicopterus and Phoenicoparrus. The similarity
between Cladorhynchus and Phoeniconaias is never-
theless considerable and these genera differ from
the Ciconiiformes in general and the storks in
particular, as in that group the accessory part is
gistrocnemius
part medialis
pars inttrmcdia
FIGURE 7.?Lateral view of right hindlimb showing the disposition of the M. flexor cruris
lateralis complex in Cladorhynchus leucocephalus (a) and Phoeniconaias minor (b).
28 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 8.?Right hindlimb of Phoeniconaias minor with M.
flexor cruris lateralis reflected outward to reveal its medial
surface and the connection with M. flexor cruris medialis.
This connection is absent in Cladorhynchus.
only a vestigial bundle of fibers that does not
insert on the femur at all (Vanden Berge, 1970).
In the condition of the raphe and the loss of the
connection with the medial flexor, Cladorhynchus
seems more specialized than any of the flamingos,
Ciconiiformes, or more typical shorebirds.
M. flexor cruris medialis
(' 'semimembranosus'')
This muscle arises fleshy from the ventral (pu-
bic) margin of the ischium, overlying the pubis
behind the obturator foramen. It is a broad ta-
pering strap that inserts by a tendon on a short
ridge on the medial surface of the shaft of the
tibiotarsus, about 1 cm distal to the medial artic-
ular facet. Vanden Berge (1970) notes that in
flamingos the medial flexor is extremely wide
proximally compared with other Ciconiiformes.
Without seeing these forms ourselves it is difficult
to evaluate the condition in Cladorhynchus, but the
muscle is nevertheless quite wide proximally.
M. ischiofemoralis
This arises fleshy from most of the concavity
caudal to the acetabulum, including the mem-
brane of the ilioischiatic fenestra. It inserts both
tendinous and fleshy on the caudo-lateral surface
of the trochanter, caudal to the insertion of M.
iliofemoralis externus. In agreement with flamin-
gos, storks, and ibises, and in contrast to herons
and Balaeniceps, it lies cranial to M. flexor cruris
medialis.
M. obturatorius medialis et lateralis
^'obturator internus et externus")
In Cladorhynchus, as in all the families examined
by Vanden Berge (1970) except the Ardeidae, the
two muscles are fused and cannot be separated.
The major part forms an elongate oval arising on
the medial side of the pelvis from the margins of
the ischio-pubic fenestra. It passes through the
obturator foramen and inserts fleshy on the cau-
dal aspect of the trochanter.
M. pubo-ischiofemoralis
("adductor longus et brevis")
Pars lateralis and pars medialis are fused prox-
imally so as to be indistinguishable; they originate
from a broad tendon on the cranio-ventral por-
tion of the ischium, covering the ischio-pubic
fenestra and the corresponding portion of the
pubis. The insertion is fleshy on the caudomedial
surface of the shaft of the femur above the pop-
liteal fossa, the fibers coalescing distally with the
combined flexor cruris lateralis pars accessoria
and gastrocnemius pars intermedia, which inserts
farther distally. The fused heads are found in
flamingos and all Ciconiiformes except herons,
whereas the fleshy insertion in Cladorhynchus is
most similar to that described for flamingos (Van-
den Berge, 1970).
M. fibularis [peroneus] longus
This muscle arises from a broad aponeurosis
over the entire tibial head and underlying mus-
culature, but is most strongly attached to the rim
of the inner, and tip of the outer, cnemial crests.
Distally the belly is divided by a long tendinous
area. The tendon extends down the lateral surface
of the tibial shaft, sends off an aponeurotic at-
tachment to the posterior rim of the internal
condyle and continues diagonally over the lateral
surface of the intertarsal joint and lateral to the
hypotarsus to insert just distal to the hypotarsus
on the tendon of M. flexor perforatus digiti III.
NUMBER 316 29
Vanden Berge (1970) indicates that in flamingos
and Ciconiiformes other than herons, the origin
from the tibial crest and most of the fibula is
fleshy, which is not true of Cladorhynchus.
M. fibularis [peroneus] brevis
Absent in Cladorhynchus. This muscle is present
in all Ciconiiformes except storks and flamingos,
a fact that has often been mentioned in the
literature (see references in Vanden Berge, 1970:
343). Its absence in Cladorhynchus, and also in
Recurvirostra (George and Berger, 1966), negates
one more supposed storklike character of flamin-
gos. Hudson's manuscript notes (fide Vanden
Berge) indicate this muscle to be unilaterally
present in Recurvirostra americana, and absent in R.
novaehollandiae, Himantopus, and certain other
Charadrii.
M. gastrocnemius
In Cladorhynchus this muscle arises from four
entirely separate heads (Figure la). The common
tendon of the four heads is the most superficial
on the caudal surface of the shank and inserts on
the hypotarsus.
PARS MEDIALIS ("INTERNA").?This originates
fleshy from the entire medial surface of the inner
cnemial crest, extending over onto the patellar
tendon so as to obscure the insertions of M.
iliotibialis cranialis and medialis.
PARS INTERMEDIA ("MEDIA").?This originates
fleshy from the popliteal fossa in common with
the fused accessory part of the lateral crural
flexor. It becomes tendinous and inserts on the
distal margin of pars medialis about three-fourths
the length of the latter.
PARS LATERALIS ("EXTERNA").?This arises
fleshy from the lateral supracondylar crest of the
femur, being overlain by M. femorotibialis exter-
nus and overlying the iliofibular loop. It fuses
with the fourth head to form a tendon that in
turn fuses midway down the shank with the
tendon of pars medialis.
"FOURTH HEAD. '?This slender muscle arises in
the popliteal fossa from a long, narrow tendon
separate from, and distal to, the origin of the
combined pars intermedia and accessory lateral
crural flexor. It inserts distally on pars lateralis
about 6 mm before the latter becomes tendinous.
The four-headed gastrocnemius is also reported
from storks, ibises, and flamingos, but does not
occur in herons or Balaeniceps (Vanden Berge,
1970). In flamingos the pars medialis covers the
anterior surface of the knee and the entire patellar
tendon and meets the proximal edge of pars
lateralis laterally. This is not true of Cladorhynchus
but may well be a size-related factor. We noted
also that in Phoeniconaias there was considerably
more distal fusion of the heads of the gastrocne-
mius, these being less easily separated and distin-
guished than in Cladorhynchus.
Digital Flexors
Vanden Berge (1970) notes that at least some
of the various flexor muscles of the toes have
fleshy origins from the shaft of the fibula in all of
the Ciconiiformes but not in the Phoenicopteri-
dae. In Cladorhynchus, as in flamingos, there is no
fleshy attachment between any of the flexors and
the shaft of the fibula.
M. flexor perforans et
perforatus digiti II
This muscle arises from two distinct heads, one
originating by a short tendon on the articular
capsule opposite the lateral condyle of the femur
and the other head from a broad, thin aponeu-
rotic sheet partly coextensive with the patellar
tendon and partly covering the origin of M.
fibularis longus. Some of the deep fibers along
the midline fuse with those of the underlying M.
flexor perforans et perforatus digiti III. The ten-
don runs through the deepest, most medial,
groove of the hypotarsus and the insertion is
similar to that in flamingos and ciconiiforms.
Flamingos agree with Cladorhynchus and differ
from all Ciconiiformes in having this muscle dou-
ble-headed instead of single-headed.
M. flexor perforans et perforatus digiti III
This can also be considered as having two
heads, though these are more intimately con-
nected than in the preceding muscle. The caudal
head is fleshy and arises from the head of the
30 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
fibula and possibly from the lateral collateral
ligament between the fibula and the distal end of
the femur. The cranial head arises partly from
the disto-lateral surface of the patellar tendon,
overlying that portion contributed mainly by M.
femorotibialis externus, and is most strongly at-
tached to the tip of the lateral cnemial crest.
There is a weak vinculum with M. flexor perfor-
atus digiti III about 1 cm above the trochlea and
the insertion is typical. Again, flamingos agree
with Cladorhynchus and differ from Ciconiiformes,
in all of which this muscle has but a single head.
Mm. flexores perforati
Of the three perforated flexors, that for digit
IV is the most superficial and that for digit II is
the deepest. These three muscles are fused proxi-
mally and are all essentially double-headed, with
the heads diverging around the insertion of M.
iliofibularis. The superficial or lateral heads of IV
and II take a common origin tendinously from
the head of the fibula. The lateral portion of III
attaches to the belly of II. The three fused deep
or medial heads take their origin fleshy from the
depths of the popliteal fossa, distal to the inser-
tions of the accessory lateral crural flexor and the
intermediate and fourth heads of the gastrocne-
mius. The deep surface of M. flexor perforatus
digiti II fuses partly with the belly of the much
smaller M. flexor hallucis longus. The tendon of
IV becomes thickened at the level of the trochlea
and is perforated at the level of the base of the
toe; it gives rise to paired insertions at the distal
ends of each phalanx. The tendon of III receives
the tendon of M. peroneus longus and continues
on to receive another, but weaker, vinculum from
M. flexor perforans et perforatus digiti III about
0.5 cm above the trochlea. This vinculum is also
present in flamingos and all ciconiiforms except
the Ardeidae. The tendon of III is perforated in
the middle of the basal phalanx and bifurcates to
insert on the ventral corners of the base of pha-
lanx 2. The tendon of II inserts as a thickened
capsule at the base of phalanx 1 digit II.
M. flexor hallucis longus
Although the hallux is absent, its flexor is
present and has a partly fleshly origin medial to
the distal attachment of the iliofibular loop.
There is a short tendinous attachment to the most
caudolateral protruberance of the lateral condyle
of the femur and the origin is fleshy medial to
this; the fleshy origin continues from a raphe
extending distally on the deep surface of M. flexor
perforatus digiti II. The belly is very short, flat,
and triangular. The slender tendon runs through
the lateral side of the tibial cartilage and through
a groove in the lateral crest of the hypotarsus.
About 1 cm or less distal to the hypotarsus it fuses
with the tendon of M. flexor digitorum longus.
This corresponds to the type IV condition of the
deep flexor tendons, according to the terminology
of Gadow (1896). This condition is found in a
number of often unrelated birds in which the
hallux is absent or greatly reduced. It occurs in
flamingos but in none of the Ciconiiformes.
M. flexor digitorum longus
This is the deepest muscle on the caudal aspect
of the shaft of the tibiotarsus. One head arises
fleshy from the head of the fibula and the proxi-
mal third of its shaft. The other head extends
medially on the shaft of the tibiotarsus alongside
the origin of M. plantaris. The tendon is the
deepest one passing through the sulcus between
the two crests of the hypotarsus; it receives the
tendon of M. flexor hallucis longus just distal to
the hypotarsus. At the distal end of the tarso-
metatarsus it trifurcates and inserts on the three
digits. The significance of the deep flexor tendons
is discussed above.
M. popliteus
This small muscle arises from the head of the
fibula deep to all other muscles. It runs diagonally
to attach disto-medially on a small protru-
berance on the caudal face of the proximal end
of the shaft of the tibiotarsus. Flamingos agree
with Cladorhynchus and differ from all Ciconi-
iformes in having the insertion of M. popliteus
distal to the origin (cf. Vanden Berge, 1970).
Intrinsic Muscles of the Tarsometatarsus
Because of the extremely slender shaft and the
absence of the hallux, the muscles originating on
NUMBER 316
the tarsometatarsus in Cladorhynchus are greatly
reduced or absent (true also of flamingos),
whereas most of these muscles are much better
developed in all Ciconiiformes. As in the case of
the deep flexor tendons, it would be easy to argue
that similarities in these respects between Clado-
rhynchus and flamingos could be due to indepen-
dent reduction of the hallux, yet it must be
remembered that this has never occurred in the
Ciconiiformes. In some cases we have not made
comparisons when Vanden Berge (1970) has not
specifically described the condition in flamingos.
M. extensor hallucis longus
Absent in Cladorhynchus and flamingos except
Phoenicopterus, where it is stated to be present but
vestigial (Vanden Berge, 1970). It is well-devel-
oped in Ciconiiformes.
Mm. extensores brevi
M. extensor brevis digiti III and M. extensor
brevis digiti IV arise from a bundle of connective
tissue just distal to the lateral cotyla on the dorsal
face of the tarsometatarsus. They appear to have
very few muscle fibers associated with them. That
for digit IV is the most lateral but its long tendon
then runs deep to that of digit III and is closely
bound to the face of the shaft of the tarsometa-
tarsus; where it enters the distal foramen it is
covered by the expanded sheath of the tendon of
III. The long tendon of M. extensor brevis digiti
III runs deep to that of M. extensor digitorum
longus; above the distal foramen it fans out into
a broad sheath covering most of trochleae III and
IV and having its insertion at the bases of their
phalanges. Vanden Berge (1970) does not give
many details of these muscles in flamingos but it
is evident that they are better developed in Ci-
coniiformes.
M. abductor digiti II
This is a fleshy muscle on the medial aspect of
the distal fifth of the tarsometatarsus. It inserts
on the base of phalanx 1 digit II.
M. flexor hallucis brevis
This tiny muscle arises as a wisp of fibers
descending from the ligamentous distal extension
of the medial crest of the hypotarsus. The belly is
about 8 mm long and the exceedingly slender
thread of a tendon extends distally on the medial
margin of the shaft of the tarsometatarsus and
appears to lose itself in the belly of M. abductor
digiti II. This muscle is also vestigial in flamingos,
in which, however, it appears to arise farther
distally. It is better developed in all Ciconi-
iformes.
M. adductor digiti II
This arises lateral to M. flexor hallucis brevis
from the distal end of the lateral crest of the
hypotarsus and adjacent surface of the tarso-
metatarsus, tapering for 13 mm before becoming
tendinous. The long tendon inserts on the medial
side of the base of phalanx 1 digit II. This muscle
also arises proximally in flamingos and ibises,
whereas in Ciconiiformes it is more distally lo-
cated.
M. lumbncalis
Not detected in Cladorhynchus and quite vesti-
gial in flamingos and in Ciconiiformes, except
herons (Vanden Berge, 1970).
M. abductor digiti IV
The tendon of insertion attaches on the lateral
corner of the plantar aspect of phalanx 1 digit IV
and runs the length of this short tapering muscle.
The fibers are oriented obliquely from this tendon
to the distal fifth of the lateral side of the plantar
face of the tarsometatarsus. This is about as de-
scribed for flamingos and storks and differs from
the condition in herons (Vanden Berge, 1970).
Pterylosis
To Nitzsch (1867:132), the pterylosis of fla-
mingos was "perfectly Stork-like," a statement
with which Gadow (1877) agreed and which has
been repeated without corroboration ever since.
On the contary, we found the pterylosis of fla-
mingos to be quite different from that of storks.
Nitzsch's great opus, which was published post-
humously, is the original and only class-wide
study of comparative pterylosis. Unfortunately, it
has never been superceded by a more modern
32 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
and comprehensive analysis. Nitzsch first con-
trasted his family Pelargi (Ciconiidae and Scopi-
dae) with the Erodii (Ardeidae) and showed the
rather generalized pterylosis of storks to be quite
different from the peculiar pterylosis of herons.
He then discussed the "Odontoglossae" (=
Phoenicopteridae) and found the pterylosis of
flamingos to be of a more usual pattern and
therefore "perfectly Stork-like" (as compared to
herons, one may assume).
Mary H. Clench (in litt. to Olson, 8 December
1978) states that "the only valid approach to
pterylography is a study of the tract patterns?
how the feathers are arranged in rows, the rela-
tionship of the rows to each other, the numbers
and lengths of rows (to a lesser extent)?in other
words, what one can see within a tract, not just its
general outlines (and resulting apteria)." Neither
our brief inquiry into pterylosis, nor the studies
of Nitzsch for that matter, meet these require-
ments. Our observations and illustrations (Figure
9) are intended solely to show that there is little
reason to regard the pterylosis of flamingos as
being storklike. We emphasize that the following
is not intended as a proper pterylographic anal-
ysis.
To investigate pterylosis, we examined fluid-
preserved specimens of Phoeniconaias minor, Ciconia
abdimit, and Cladorhynchus leucocephalus, from which
we had clipped the feathers. All of these speci-
mens had been partially dissected, obscuring the
configuration of the feather tracts in certain areas,
particularly the abdomen in the flamingo and
stork, and the neck and ventral midline in Clado-
rhynchus. Terminology follows that of Lucas and
Stettenheim (1972).
The great density both of contour feathers and
down in Phoeniconaias and Cladorhynchus (Figure 9)
contrasts markedly with the sparse feathering and
reduced down of Ciconia. In Ciconia the neck is
feathered in two lateral bands separated by wide
ventral and dorsal apteria; the latter is an anterior
extension of the interscapular apterium. The two
cervical apteria extend two-thirds the length of
the neck, the remainder of which appears to be
nearly continuously feathered all around. Phoeni-
conaias and Cladorhynchus have the neck much
more densely clothed in feathers and down than
in Ciconia. There appears to be no dorsal cervical
apterium or ventral cervical apterium in Clado-
rhynchus. Only the latter is present in Phoeniconaias;
it is much smaller than in Ciconia and extends for
less than one-fourth the length of the neck. In
Cladorhynchus, a small lateral cervical apterium
lies on each side of the base of the neck. These
are absent in Phoeniconaias and Ciconia.
Ciconia has a rather wide sternal apterium; this
is narrower in Phoeniconaias and we could not
detect it in our specimen of Cladorhynchus, which,
however, had previously been cut down the mid-
line. The pectoral tract in Ciconia is broad and
clothed with regularly spaced, sparse, weak feath-
ers. Phoeniconaias and Cladorhynchus are much more
densely feathered and have several rows of closely
spaced, large, stiff-shafted feathers in the dorsal
portions of the tract. Cladorhynchus differs from
Phoeniconaias in having pectoral apteria that de-
limit a median tract, in which, as mentioned, the
sternal apterium of our specimen was absent or
destroyed.
In Cladorhynchus and Phoeniconaias, the femoral,
crural, and dorsal caudal tracts are nearly contin-
uously and rather densely feathered, and several
longitudinal rows of stiffer feathers occur along
the ventral margin of the pelvis above the crus.
This differs from Ciconia, in which the dorsal
caudal tract consists of a few rows of sparse
feathers separated from the femoral tracts by
lateral pelvic apteria. Ciconia also has crural ap-
teria, which appear to be lacking in Cladorhynchus
and Phoeniconaias. The uropygial gland is dis-
tinctly tufted in Phoeniconaias and Cladorhynchus
and nearly bare in Ciconia. David W. Johnston,
(in litt. to Olson, 17 October 1978) found this
gland in Phoenicoparrus to be more similar to that
of Himantopus than to that of either Mycteria (Ci-
coniidae) or Anas (Anatidae).
In dorsal view (Figure 9), the humeral tracts in
Cladorhynchus and Phoeniconaias are broad, elongate
patches of extremely densely packed and very
stiff feathers; in contrast, this tract in Ciconia is
smaller and consists posteriorly of a few very large
feathers and anteriorly of sparse, weak feathers.
As previously noted, there are 11 primaries in
NUMBER 316 33
Oodorhynchus
FIGURE 9.?Semidiagramatic views contrasting the pterylographic patterns of a stork (Ciconia
abdimu), flamingo {Phoemconaias minor), and the Australian Banded Stilt (Cladorhynchus leucoce-
phalus). (Question marks indicate those areas in our specimens that were destroyed by previous
dissections. These drawings are intended only to show basic patterns and do not accurately
represent the distribution of feathers within tracts.)
34 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
storks and flamingos. Cladorhynchus has 10. Of
secondaries (counting tertials) there are 19 in
Cladorhynchus, 20 in Ciconia, and 25 in Phoeniconaias.
This, along with the general proportions of the
wing, suggests that the entire wing in flamingos
has become elongated, which could account for
the greater number of secondaries and the addi-
tion of a primary. This has coincidentally resulted
in flamingos having the same number of primar-
ies as storks, whereas the number of secondaries
is considerably greater.
There are substantial differences in pterylosis
between all three of the forms we examined.
There is at least some similarity between Clado-
rhynchus and Phoeniconaias in the density of feath-
ering, particularly of the neck and pectoral and
humeral tracts. This could represent an indepen-
dently evolved response to the caustic habitat in
which each lives. We conclude only that the
pterylosis of flamingos cannot be said to be stork-
like.
Natal Down
The literature on natal down contains consid-
erable misleading information. The subject is of
importance here because the natal down of fla-
mingos has been said to be like that of storks. The
following summary is largely an outgrowth of
correspondence with Kenneth C. Parkes, to whom
we are indebted for supplying unpublished obser-
vations.
In the young of certain birds there may appear
to be two successive coats of down, i.e., two sets
of downy growth emerging sequentially from the
same set of feather follicles. This is strictly true
only of a limited number of taxa such as Procel-
lariformes, Gaviiformes, and Sphenisciformes. In
most other such birds the second coat of down is
actually the very plumulaceous tips of the emerg-
ing juvenal plumage.
The Anseriformes and Charadriiformes have a
single coat of natal down, whereas the Ciconi-
iformes and flamingos, are thought to have two,
although it is known that herons have but one
(Palmer, 1962). The condition in the Scopidae
and Balaenicipitidae is unknown to us. Although
ibises (Threskiornithidae) are said to have two
coats of down (Palmer, 1962), the supposed sec-
ond coat is body down that grows from different
follicles (Parkes, in litt. to Olson, 27 November
1978). Storks and flamingos have a second coat
of down formed by the tips of the juvenal plu-
mage. Sibley et al. (1969) gave considerable em-
phasis to this character in attempting to show
ciconiiform affinities for flamingos.
In two fluid-preserved specimens of downy
chicks of Cladorhynchus, we found clear evidence
of two successive stages of down, the first of which
could still be seen attached to the second (Figure
10). Feather growth in these specimens was insuf-
ficient to ascertain whether the second set of
down was actually the tips of the juvenal plu-
mage, however we assume this to be the case. No
other member of the Charadrii is known to have
two coats of natal down. The white coloration
and lack of markings in the downy young of
Cladorhynchus are likewise unique in the Charadrii
(page 11). In view of all the other flamingo-like
attributes of Cladorhynchus, the nature of its natal
down assumes considerable significance. The con-
dition of the natal down in flamingos, therefore,
is at least as similar to that of Cladorhynchus as it
is to that of storks.
Oology
The eggs of flamingos are large relative to the
size of the bird and this is likewise one of the
striking features of the eggs of Cladorhynchus. Al-
though Cladorhynchus leucocephalus is somewhat
smaller than Recurvirostra americana, its eggs are
much larger (Figure 11). The weight of the egg of
C. leucocephalus taken as a percentage of body
weight is twice that of R. americana (Table 2). The
same is true of the flamingo Phoenicopterus ruber,
versus the stork Mycteria americana; both of these
birds are about the same size, yet the relative egg
size of the flamingo is twice that of the stork
(Table 2). Naturally, because of allometric effects,
the relative size of the eggs is smaller in the larger
birds (the body weight of the flamingo is ten
NUMBER 316 35
FIGURE 10.?Feather from a chick of the Australian Banded Stilt, Cladorhynchus leucocephalus,
showing (a) the "two coats of down," the upper portion being true down and the lower probably
being the plumulaceous tip of the juvenal feather, as in flamingos, and (b) further enlarged
view of same to show the juncture of the first and second coat of down.
36 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 11.?Comparison of the pelves (top) and eggs (bot-
tom) of the Australian Banded Stilt, Cladorhynchus leucoce-
phalus (a), and American Avocet, Recurvirostra amencana (b),
to show the disproportionately large size and light color of
the egg of Cladorhynchus.
times that of Cladorhynchus and its egg weight
obviously could not increase by a like proportion).
The large egg size in Cladorhynchus and flamingos
is probably correlated with the need to produce
large well-developed young that are better able
to survive in a harsh and often ephemeral habitat.
Flamingo eggs are white, unmarked, and cov-
ered with a rather thick chalky coat that is absent
TABLE 2.?Relative egg weights of two recurvirostrids, a
flamingo, and a stork (all weights in grams; averages of egg
weights obtained from water filled egg-shells (n = 3, except
Cladorhynchus, n = 2); body weights are averages: Recurvirostra,
17 females (Hamilton, 1975); Cladorhynchus, 2 unsexed
(McNamara, 1976); Phoenicopterus, 3 males and 2 females
(Rooth, 1965); Mycteria, 2 males (Palmer, 1962))
Species
Recurvirostra americana
Cladorhynchus leucocephalus
Phoenicopterus ntber
Mycteria americana
Body
weight
Egg
weight
Egg weight
as %of
body weight
310
238
3050
3171
30
44
160
86
9.7
18.5
5.2
2.7
in storks and shorebirds. As mentioned, the
ground color of the eggs of Cladorhynchus is pecu-
liar among the Charadrii in being white, and
markings may occasionally be absent (Figure 12).
Although McGilp and Morgan (1931:44) de-
scribe the texture as "chalky," there is no powdery
coating as in flamingos.
We examined the surface structure of the egg-
shell of Recurvirostra, Cladorhynchus, Phoenicopterus,
and Ciconia with a scanning electron microscope,
first removing the powdery layer from the fla-
mingo egg with a small buffing wheel. The two
recurvirostrids and the flamingo exhibit a rather
uniform granular structure that is significantly
different from that of Ciconia, in which the surface
of the shell is regularly pitted with distinct pores
(Figure 13), a condition long recognized as being
typical of storks (Des Murs, 1860). We conclude
from this only that the eggs of storks bear no
resemblance to those of flamingos.
Even if the distinctive attributes of the eggs of
Cladorhynchus evolved independently of those of
the Phoenicopteridae, this at least demonstrates
that a flamingo-like condition can be derived
from that of the Charadrii.
Parasitology
Sibley et al. (1969:162) reviewed the literature
on the parasites of flamingos but concluded only
that this evidence was "as conflicting and difficult
to interpret as is that from morphology."
NUMBER 316 37
FIGURE 12.?Eggs of the Australian Banded Stilt, Cladorhynchus leucocephalus, to show variation
in markings, which may occasionally be absent. (Photograph from McGilp and Morgan, 1931.)
Concerning the cestode parasites, the remarks
of Baer (1957:274) are of considerable interest:
"One finds in flamingos four monotypic, endemic
genera (Amabilia, Cladogynia, Gynandrotaenia, Lep-
totaenia). The last two, very specialized overall,
are derived from a family of cestodes character-
istic of the Charadrii" (our translation). Baer
(1951, 1957) has argued that the high degree of
host specificity of cestodes renders them useful for
assessing phylogenetic relationships of hosts. The
evidence in this case is neither conflicting nor
difficult to interpret, as it agrees with the hypoth-
esis of charadriiform origins of flamingos.
The mallophagan ectoparasites of flamingos,
however, present a different picture. Hopkins
(1942:102) reported that flamingos are parasi-
tized by three genera of feather lice that occur
elsewhere only on the Anseriformes. He regarded
this "as complete proof that the Flamingos are
Anseriformes, and even that their divergence
from the stock that gave rise to the Anatidae took
place at no very remote period of time." However,
K. C. Emerson (pers. comm.) has indicated to us
that the species ofAnatoecus, Anaticola, and Triniton
found on flamingos differ from those found on
the Anatidae to a degree that would suggest their
divergence did not occur recently.
Some authors have considered host transfer of
Mallophaga to be frequent (Mayr, 1957; Strese-
mann, 1959), suggesting that flamingos "have
acquired their feather lice from the Anatidae
since they have lived in the same environment
. . . " (Sibley et al., 1969:162). This seems oversim-
plified and were this often the case, one would
expect most waterbirds to have the same kinds of
Mallophaga.
The evolutionary history of flamingos and the
Anseriformes suggests a logical possibility for
transfer of Mallophaga that transcends mere
chance. Modern flamingos nest in dense colonies
in harsh, saline environments, and therefore,
when breeding, are actually relatively isolated
from other birds. The available evidence indicates
that the same was probably true of early flamin-
38 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 13.?Scanning electron micrographs of eggshell surface: a, stork, Ciconia nigra; b,
flamingo, Phoenuopterus ruber; c, Australian Banded Stilt, Cladorhynchus leucocephalus; d, avocet,
Recurvirostra americana. Note the distinctly pitted surface in the stork as opposed to the unpitted,
granular surface in the others. (Scale = 1 mm. Photographs by Mary Jacque Mann.)
gos (page 48). As represented by Presbyornis, the
ancestors of the Anseriformes were likewise ex-
tremely colonial shorebirds that lived in the same
kinds of habitat (Olson and Feduccia, in press).
For at least part of their history, flamingos were
probably contemporaneous with Presbyornis. Op-
portunity for transfer of Mallophaga from outside
sources would presumably have been reduced due
to the lack of other species of birds adapted to
such a harsh environment. On the other hand,
NUMBER 316
one may readily imagine that the often ephemeral
nature of suitable breeding sites might at times
have caused colonies of flamingos and Presbyornis
to be situated adjacent to one another, or they
may even have bred in mixed colonies. Densely
packed, mixed flocks of flightless downy young
could have resulted from such a juxtaposition,
and would have provided ample opportunity for
transfer of ectoparasites. Thus, the similarity of
anseriform and phoenicopterid Mallophaga is not
necessarily due to a close relationship of the hosts,
but to the fact that the ancestors of these two
groups shared similar specialized habits and hab-
itat and were in intimate contact with each other
as a consequence.
Specimens of Mallophaga from Cladorhynchus
were kindly forwarded to us by Shane Parker of
the South Australian Museum. They were iden-
tified as belonging to the genera Actornithophilus,
Austromenopon, and Quadraceps, which are charac-
teristic of the Charadriiformes (K. C. Emerson,
pers. comm.). Thus, the Mallophaga of flamingos
must have been acquired subsequent to their
divergence from the Recurvirostridae.
A charadriiform origin of flamingos provides a
concordant explanation for the parasites they
harbor, whereas parasitology provides no evi-
dence in favor of a relationship between flamingos
and the Ciconiiformes.
Biochemistry
Biochemical information from several sources
has been used in attempts to determine the rela-
tionships of flamingos. Mainardi (1962) investi-
gated red-cell antigens; Sibley (1960) used paper
electrophoresis to compare egg-white proteins;
and Sibley et al. (1969) studied starch-gel electro-
phoresis of egg-white proteins and hemoglobins,
tryptic peptides of hemoglobins, and thin-layer
electrophoresis of tryptic peptides of ovalbumin.
Sibley and Ahlquist (1972) reviewed the egg-
white protein evidence for non-passerine birds,
including flamingos. These investigations ante-
dated the use of the isoelectric focussing technique
(see Sibley and Frelin, 1972), which results in
more detailed patterns somewhat more suscepti-
ble to evaluation by the uninitiated. Brush (1979)
has recently shown that there were serious pro-
cedural difficulties inherent in Sibley's electro-
phoretic methodology that render dubious the
results obtained.
Regardless, these biochemical investigations
are unfortunately uninformative for interpreting
the relationships of flamingos because all com-
parisons were conducted with the traditional idea
in mind that flamingos must be related either to
storks or to ducks. Sibley et al. (1969) concluded
that the biochemical evidence showed flamingos
to have more in common with Ciconiiformes than
Anseriformes, but in the absence of any meaning-
ful comparisons with Charadriiformes, particu-
larly the Recurvirostridae, such a conclusion has
little significance. As long as biochemistry is used
in avian systematics merely to legitimize precon-
ceptions based on the incomplete anatomical
studies of the nineteenth century, its usefulness as
a taxonomic tool is bound to remain severely
limited.
Osteology
Feduccia (1976) discussed and illustrated osteo-
logical features of flamingos that indicate rela-
tionships to the Charadriiformes rather than Ci-
coniiformes. These observations are augmented
below. Because even with the removal of the
Phoenicopteridae from the Ciconiiformes, the or-
der is still probably hopelessly unnatural (Olson,
1979), and because storks in particular have most
often been mentioned as relatives of flamingos,
we have confined our comparisons to the Cicon-
iidae. Terminology generally follows Howard
(1929).
SKULL
Despite the great modification of the skull in
flamingos, the architecture of the palate is decid-
edly not like that of a stork (Figure 14). The
palatines of flamingos are longer and narrower
and the pterygoids shorter and more expanded
anteriorly than those of storks, thus resembling
shorebirds. The choanal aperture extends poste-
riorly to the palatine-pterygoid articulation in
flamingos and shorebirds, whereas it ends consid-
40 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
erably anterior to this in storks. The posterior
margin of the palatine curves gently into the
articulation with the pterygoid in flamingos and
shorebirds, whereas in storks it is sharply truncate
and the palatines become much narrower before
articulating with the pterygoid (Figure 14). The
fact that the palatines in flamingos have fused
along the midline ("desmognathy"), as in storks,
seems of relatively minor importance compared
with the otherwise great differences in the palates
of these birds.
In his studies of the middle ear region of the
skull, Saiff (1978) found that the Phoenicopteri-
dae differed significantly from other families of
"Ciconiiformes," though he made no comparisons
with the Charadrii.
A character in the skull of flamingos that is
probably of greater taxonomic significance than
previously thought is the presence of distinct
paired occipital fontanelles above the foramen
magnum. These are characteristic of most Char-
adrii and certain Alcidae; they are present in
most Anseriformes, which were in turn derived
from the Charadrii formes (Olson and Feduccia,
in press). In the Gruiformes, occipital fontanelles
occur solely in the closely related Aramidae and
Gruidae, which may be among the more derived
members of the order. Elsewhere, these apertures
are found only in the ibises, Threskiornithidae,
which are probably a transitional group between
FIGURE 14.?Semidiagramatic ventral view of palate:
a, stork, Cicoma episcopus; b, flamingo, Phoemcopterus ntber;
c, recurvirostrid, Cladorhynchus Uucocephalus. The flamingo, as
would be expected from the unique feeding apparatus,
differs from either of the others, but is less similar to the
stork. Note particularly the distinctive constriction of the
palatines (pi) before they contact the pterygoids (pi) in the
stork.
Gruiformes and Charadriiformes (Olson, 1979).
The presence of occipital fontanelles in flamingos
is best interpreted as a derived character shared
with the Charadrii.
POSTCRANIAL SKELETON
In the following characters of the postcranial
skeleton, flamingos agree with Recurvirostridae
and differ from the Ciconiidae.
CORACOID.?(1) Shaft much shorter and
stouter; (2) procoracoid larger, projecting farther
medially, perforate (except in Cladorhynchus); (3)
acrocoracoid narrower and much more elevated
above the glenoid facet; (4) furcular facet a dis-
tinct, flat, rectangular surface; (5) sternal margin
curved, not straight; (6) sternal facet much
longer, not confined to medial half of sternal end;
(7) sterno-coracoidal process deeper and more
truncate. In most shorebirds, the brachial tuber-
osity and furcular facet are more extensive than
in flamingos (Figure 15); this area has been noted
by Strauch (1978:309, fig. 21) to be variable in
the Charadriiformes. Its reduction in flamingos
may well be correlated with the changes in the
proximal end of the humerus and the associated
modification of the shoulder musculature.
SCAPULA.?(1) Acromion long and pointed, not
square and blunt; (2) shaft narrower proximally.
B
FIGURE 15.?Ventral view of left coracoid: a, stork, Cicoma
abdimu; b, flamingo, Phoemcopterus ruber; c, recurvirostrid,
Recurvirostra americana.
NUMBER 316 41
FURCULA.?(1) Narrow, U-shaped, with clavi-
cles parallel, not diverging dorsally; (2) scapular
tuberosity longer, narrower, and more pointed;
(3) hypocleidium very small, not approaching
carina (in storks the hypocleidium is very large
and articulates by a large facet at the anterior
end of the sternal carina; see Figure 16c).
STERNUM.?(1) Longer and narrower; (2) car-
ina does not project anteriorly beyond the man-
ubrium; (3) manubrium a deep blade, not a
simple peg-like process (Figure 16; see also Fed-
uccia, 1976, fig. 6).
HUMERUS.?(1) Bicipital crest long, tapering
gently into shaft, not jutting out abruptly; (2)
scar for attachment of M. pectoralis not lying
mainly distal to deltoid crest; (3) entepicondylar
prominence poorly developed; (4) olecranal fossa
narrow and distinct; (5) scar for M. latissimus
dorsi posterioris lying ventral to midline of shaft,
not dorsal as in storks; (6) distal end relatively
A A
FIGURE 16.?Outline of furcula in anterior view (left col-
umn) and left lateral view of sternum, coracoid, and furcula
(right column): a, recurvirostrid, Cladorhynchus leucocephalus\
b, flamingo, Phoenicopterus ruber; c, stork, Ciconia episcopus. Note
the large hypocleidium of the furcula in the stork and its
solid articulation with the apex of the carina.
narrower.
CARPOMETACARPUS.?(1) Metacarpal I more
proximally directed, less vertical; (2) ventro-
medial rim of carpal trochlea less prominent;
(3) proximal metacarpal symphysis much shorter;
(4) metacarpal III straight, not bowed ventrally;
(5) distal metacarpal symphysis relatively longer.
PELVIS.?(1) Anterior iliac shield not markedly
expanded anteriorly; (2) postacetabular ilium not
fused to synsacrum; (3) obturator foramen rela-
tively smaller.
FEMUR.?(1) Proportionately shorter and
stouter; (2) anterior and proximal extent of tro-
chanter greater; (3) configuration of muscle scars
on proximo-lateral surface similar in flamingos
and recurvirostrids and quite distinct from that
of storks; (4) anterior rim of internal condyle
extends farther anteriorly and proximally; (5)
internal condyle in medial view more pointed;
(6) rotular groove deeper. It should be noted that
the femur in Cladorhynchus is stouter and more
flamingo-like than in Recurvirostra or Himantopus.
TIBIOTARSUS.?(1) Inner cnemial crest much
more extensive anteriorly, appearing squared in
medial view (see Feduccia, 1976, fig. 2); (2) inner
cnemial crest extends proximally far above level
of outer cnemial crest, whereas in storks the crests
are at about the same level (Figure 17); (3) notch
FIGURE 17.?Proximal end of right tibiotarsus in anterior
view: a, stork, Ciconia abdimn; b, flamingo. Phoemconaias minor;
c, recurvirostrid, Cladorhynchus leucocephalus. Note the much
reduced inner cnemial crest (u) in the stork.
42 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
present in distal rim of internal condyle; (4)
anterior intercondylar fossa expanded proxi-
mally, not almost round as in storks (Figure 18);
(5) distal end more expanded, particularly me-
dially, with the internal ligamental prominence
larger; (6) internal condyle in medial view longer
and narrower (particularly true of Cladorhynchus,
which is most similar to the extinct genus Palae-
lodus in this respect); (7) posterior articular surface
does not extend as far proximally.
TARSOMETATARSUS.?(1) Intercotylar knob
much broader and more rounded, not notched
laterally (Figure 24); (2) shaft much more lat-
erally compressed; (3) distal foramen smaller; (4)
inner trochlea much higher and more posteriorly
rotated (Figure 24; also Feduccia 1976, figs. 3 and
4); (5) scar for hallux reduced or absent.
PHALANGES.?(1) All phalanges, including un-
guals, much shorter, wider, and deeper, whereas
in storks the phalanges, including the well-devel-
oped hallux, are long and slender.
The vertebral count and the structure of the
cervical vertebrae of flamingos differ from both
shorebirds and storks, but these modifications are
almost certainly correlated with the feeding ad-
aptations. The first three or four anterior thoracic
vertebrae are fused into a notorium in modern
flamingos, a condition absent in shorebirds and
storks but which evidently has evolved in flamin-
gos since the early Eocene (page 57). The first
thoracic vertebra in flamingos bears a large he-
mapophysis, which is true of the Recurvirostridae
but not storks, in which this process is absent.
There is a superficial resemblance between fla-
mingos and storks in the distal end of the tibi-
otarsus, in both of which there is a deep, distinct
anterior intercondylar fossa and a tubercle on the
tendinal bridge. The shape of this fossa, however,
is nearly round in storks, whereas it is expanded
proximally in flamingos, particularly on the lat-
eral side, where it incises the external condyle
(Figure 18). Furthermore, the tubercle on the
tendinal bridge of flamingos is nearly continuous
with another tubercle directly proximal to it,
FIGURE 18.?Distal end of right tibiotarsus: a, stork, Ciconia
abdimii; b, flamingo, Phoeniconaias minor. Although in both
families there is a deep intercondylar fossa, its shape, as well
as that of the rest of the element and the placement of the
tubercles is entirely different.
whereas in storks the second tubercle is separate
and lies entirely lateral to the first.
The sterna of flamingos and storks have but
two posterior notches. Most Charadrii typically
have a four-notched sternum but only two
notches occur in the Jacanidae, Rostratulidae,
Thinocoridae, and some individuals of Burhini-
dae. It is likely that the loss of the medial notches
in flamingos is a secondary development.
The proportions of the hindlimb elements of
flamingos are quite different from those of storks
and are more similar to those in the Recurviros-
tridae. As an example, the absolute length of the
femur in Phoenicopterns ruber is less than that in
Ciconia nigra, whereas the tarsometatarsus of the
flamingo is much longer than that of the stork.
Because of the number of unique non-skeletal
features shared by flamingos and Cladorhynchus, it
should be noted that the osteology of Cladorhynchus
does not differ appreciably from that of the other
members of the Recurvirostridae (Strauch, 1978;
this study) and it lacks the skeletal peculiarities
diagnostic of the Phoenicopteridae.
NUMBER 316
Significant osteological differences between fla-
mingos and shorebirds are seen, of course, in the
modification of the feeding apparatus and cervi-
cal vertebrae. These specializations are unique to
flamingos and hence cannot show relationships,
but as discussed later, they are more easily derived
from the charadriiform condition than that in
Ciconiiformes, particularly storks.
Apart from the feeding specializations, the
greatest differences between flamingos and typi-
cal Charadrii are seen in the humerus and the
shoulder joint. Many of these differences are
probably due to the pneumatization of the prox-
imal end of the humerus. This is almost certainly
a size-related phenomenon, because in almost all
birds the size of extant flamingos the humerus is
pneumatized. Comparison of the fossil frigatebird
Limnofregata (Pelcaniformes: Fregatidae) with Re-
cent species in the same family, shows the great
extent to which the humerus may be modified
with increasing pneumatization (Olson, 1977:23).
Adaptations paralleling those of flamingos, such
as the reduction of the ectepicondylar spur of the
humerus and the brachial tuberosity of the cora-
coid, are also found in the charadriiform species
Scolopax minor, whereas they are absent in other
members of the genus (Olson, 1976). The hu-
merus is not pnemumatic in 5. minor, however,
and the modifications of the wing probably
evolved in connection with sound production dur-
ing mating displays. Nevertheless, this shows that
adaptations similar to some of those in the wing
and shoulder of flamingos have evolved within a
single genus of Charadriiformes.
With the exceptions noted above, the osteology
of the Phoenicopteridae conforms very well with
that of the Charadrii. On the other hand, nothing
in their skeletal structure can be used to support
a relationship with the Ciconiiformes.
Paleontology
The fossil record of flamingos has been inven-
toried by Brodkorb (1963a) and briefly discussed
by Sibley et al. (1969). We shall review the im-
portance (or lack thereof) of the various fossils
attributed to flamingos, adding a description of
a significant new genus from the middle Eocene
of Wyoming.
A few fragments of Cretaceous bones have been
said, on very insufficient grounds, to belong to
birds related to flamingos. The earliest of these,
and one of the earliest birds known, is Gallornis
straeleni, described by Lambrecht (1931) as a new
genus of Anatidae from the Lower Cretaceous
(Neocomian) of France. This was based on "the
proximal portion of a femur and a scrap of hu-
merus, the latter of no comparative value" (Brod-
korb, 1963b:63). Using only Lambrecht's illustra-
tions for comparison, Brodkorb (1963b) decided
that Gallornis was definitely not anseriform and
he referred it to the neighborhood of flamingos,
placing it in the extinct family Scaniornithidae.
We regard it as impossible to determine the affin-
ities of Mesozoic birds with such undiagnostic
fragments; in fact, it is difficult enough and usu-
ally impossible to determine the nature even of
early Tertiary birds from such material (see Ol-
son, 1977:31).
The same applies, though even more emphat-
ically, to a single vertebra from the late Creta-
ceous (Campanian) of Sweden that Lambrecht
(1933:335) optimistically described as a flamingo
under the name Parascaniomis stensioi.
The avifauna of the late Cretaceous (Maes-
trichtian) Lance Formation, analyzed by Brod-
korb (1963b), contains what was described as a
new genus and species of flamingo, Torotix cle-
mensi, based on the distal end of a humerus (not
a "head" as stated by Sibley et al., 1969:158).
Brodkorb placed this in a new family Torotigidae,
to which he arbitrarily assigned Gallornis and
Parascaniomis.
Brodkorb (1963b) identified two other families
of birds from the Lance Formation: the Cimolop-
terygidae, an extinct family of Charadriiformes
known only from coracoids, and the Lonchody-
tidae, a family consisting of two species supposed
to belong to the Gaviiformes, and known from a
fairly diagonostic distal end of a tarsometatarsus,
as well as a fragment of carpometacarpus that we
regard as indeterminable.
44 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
After preliminary examination of much of this
material, we consider it quite possible that all of
the birds so far known from the Lance Formation
may be referable to the Charadriiformes. As evi-
denced by the following, the holotype tarsome-
tatarsus of Lonchodytes estesi is more similar to the
Charadrii than to the Gaviidae: (1) lesser lateral
compression of the shaft; (2) greater elevation of
the outer trochlea relative to the middle trochlea;
(3) lesser retraction of the inner trochlea. Professor
Brodkorb (pers. comm.) now concurs with us at
least that L. estesi is not gaviiform; we consider it
to be closest to the Charadriiformes.
The holotype of Torotix clemensi lacks the large
ectepicondylar spur typical of most Charadri-
iformes and thus resembles both the Phoenicop-
teridae and the Presbyornithidae, a charadriiform
family near the ancestry of ducks. This humerus
could well belong to one of the species of Cimolop-
teryx, known only from coracoids, while the type
of Lonchodytes estesi may be referable to one of the
larger species of Cimolopterygidae. Without bet-
ter material it probably is not possible to deter-
mine whether the Lance avifauna contains fla-
mingo-like or presbyornithid-like Charadri-
iformes, or neither.
Scaniornis lundgreni Dames (1890), from the
lower Paleocene of Sweden, is based on a hu-
merus, scapula, and coracoid. Dames' rather in-
different illustration shows these to be poorly
preserved, mostly as impressions in a slab. Al-
though nothing in his illustration rules out the
possibility that the species was a flamingo, neither
is there anything diagnostic to be seen. Until the
specimen is reprepared and restudied, its affinities
must be regarded as uncertain. The family Scan-
iornithidae proposed by Lambrecht (1933) is un-
justified and undiagnosable on the basis of avail-
able information.
The genus Telmabates from the lower Eocene of
Patagonia, was regarded by Howard (1955) as
forming a new family, Telmabatidae, having
some affinities with flamingos. Feduccia and
McGrew (1974) showed that Telmabates and Tel-
mabatidae are junior synonyms of Presbyornis and
Presbyornithidae, respectively, known from con-
temporaneous deposits in the western United
States. Most, if not all, of the flamingo-like char-
acters of these birds are actually charadriiform in
nature. We treat these charadriiform-anseriform
mosaics in another paper dealing with the origin
of the Anseriformes (Olson and Feduccia, in
press).
The genus Agnopterus was founded by Milne-
Edwards (1868) for his species A. launllardi, based
on the distal portion of a tibiotarsus lacking most
of the diagnostic features. His illustration does
not serve to confirm or deny his placement of the
genus with the flamingos. Lambrecht's (1933)
elevation of it to family rank cannot be justified
on the basis of such a specimen.
Agnopterus turgaiensis Tugarinov (1940), from
the upper Oligocene of Kazakhstan, is based on
a well preserved distal end of a tibiotarsus that
seems, on the basis of the original illustrations, to
be correctly called a flamingo. That it properly
belongs to the same genus as A. laurillardi may be
questioned, particularly as it is geologically much
younger and also nearly contemporaneous with
Palaelodus and the earliest known form of Phoeni-
copterus, with both of which it needs comparison.
Lydekker (1891) described a coracoid from the
upper Eocene of England, referring it with a
query to Milne-Edwards' genus Agnopterus as A.
hantoniensis. Harrison and Walker (1976b) referred
a humerus to this species, and made it the type of
a new genus, Headonornis, of Telmabatidae, either
overlooking or ignoring the fact that Feduccia
and McGrew (1974) had synonymized this family
with the Presbyornithidae. Harrison and
Walker's diagnosis of Headonornis does not diag-
nose the genus, nor do they explain why the taxon
was referred to the Telmabatidae or how it differs
from Telmabates (= Presbyornis). Their illustration
of the humerus shows it to be quite different from
that of flamingos, but the same may not be true
of the type coracoid. Until a proper comparative
study is made, the significance of these specimens
to the evolution of either flamingos or the Pres-
byornithidae cannot be determined.
The nomenclatural and taxonomic status of
Elorms littoralis and E. grandis, from the lower
NUMBER 316 45
Oliogocene of France, was reviewed by Olson
(1978). The specimens on which these names were
based have been lost and the taxa are now known
only from Milne-Edwards' (1867-1871) illustra-
tions and descriptions. These do not preclude
phoenicopterid affinities for these taxa, but be-
yond this little else can be said. Elornis anglicus
Lydekker, from the upper Eocene of England,
was synonymized by Harrison and Walker
(1976b) with Actiornis anglicus Lydekker, formerly
of the Phalacrocoracidae, which they then trans-
ferred to the Threskiornithidae. Any supposed
phoenicopterid affinities of this taxon are thus
doubtful.
Tiliornis senex Ameghino (1899), based on an
unillustrated coracoid from the Lower Oligocene
of Argentina and assigned to the Phoenicopteri-
dae, is a meaningless name until the type is
located and restudied.
Hitherto, the earliest unequivocal flamingos
based on sufficient material to have some evolu-
tionary significance have come mainly from late
Oligocene or early Miocene (Aquitanian) deposits
in France. These consist of an extinct species in a
modern genus, Phoenicopterus croizeti, and several
species in the extinct genus Palaelodus. Six species
of the latter have been named, mostly distin-
guished on size. Although known from abundant
material, no modern comparative study has ever
been made of Palaelodus and a revision would no
doubt result in the recognition of fewer species.
One species, Palaelodus steinheimensis Fraas (1840),
from the late Miocene of Germany, is misidenti-
fied to family, being based on what appears to be
the distal end of a tibiotarsus of a large anseriform
(Olson, pers. obs.). Species larger than any of
those of Palaelodus have been named in the genus
Megapaloelodus, from the early Miocene and early
Pliocene of North America (A. H. Miller, 1944;
Brodkorb, 1961; Howard, 1971). We have exam-
ined additional specimens of Megapaloelodus from
the middle Miocene (Clarendonian) of Texas
(AMNH 9109) and the Aquitanian of France
(USNM 18497). This genus is very similar to, and
may not be separable from, Palaelodus.
Palaelodus and Megapaloelodus are usually sepa-
rated from the Phoenicopteridae as a distinct
family, Palaelodidae. Most skeletal elements of
Palaelodus agree well with the Phoenicopteridae.
The cervical vertebrae are greatly elongated as in
modern flamingos, and the humerus is decidedly
flamingo-like as well. The specimen of bill previ-
ously assigned to Palaelodus by Milne-Edwards
(1867-71, vol. 2), was referred by Cracraft (1973:
87-88) to the gruiform species Probalaerica proble-
matical the type of which is also a bill. In our
opinion, the true identity of these Aquitanian
rostra, as well as the skull that forms the type of
the supposed ibis Ibidopodia palustris Milne-Ed-
wards, remains problematical. The latter needs
comparison with the cranium illustrated by
Rothausen (1966) that was found in association
with postcranial elements of Palaelodus. In any
case, the morphology of the bill of Palaelodus is
not certainly known.
The most obvious difference between Palaelodus
and modern flamingos is the shorter tibiotarsus
and the shorter and more laterally compressed
tarsometatarsus of the former. These modifica-
tions suggest that the species of Palaelodus may
have occupied more of a duck-like swimming
niche than do typical flamingos. The differences
in the proportions of the hindlimb between typi-
cal flamingos and Palaelodus are hardly greater
than seen between the genera of recent Recurvi-
rostridae (Figure 19). Although the osteology and
systematics of Palaelodus and Megapaloelodus re-
quire further study, we believe that they are
clearly flamingos and should be included in the
Phoenicopteridae.
Contemporaneous with Palaelodus in the Aqui-
tanian of France is a typical flamingo, Phoenicop-
terus croizeti Gervais, known from a number of
specimens, including cranial material. Harrison
and Walker (1976a) have recently proposed a
new genus, Gervaisia, with P. croizeti (which they
consistently misspell "croiseti") as the type. They
based their diagnosis solely on fragments of bill
that they happened to have on hand, evidently
without consulting any of the more diagnostic
material that is available in various other mu-
seums. As happens too frequently with Harrison
46 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 19.?Right tarsometatarsi in medial view: a, Phoent-
conaias minor, Phoenicopteridae; b, Palaelodus sp., Phoenicop-
teridae; c, Himantopus mexicanus, Recurvirostridae; d, Clador-
hynchus leucocephalus, Recurvirostridae. Note that the differ-
ence in proportions between the two genera of flamingos is
about the same as that between the two recurvirostrids.
(Scale in cm.)
and Walker, their name was preoccupied, in this
case thrice over. Kashin (1978) noted that Ger-
vaisia Bonaparte, 1854 (Aves), Gervaisia Waga,
1858 (Myriapoda), and Gervaisia Robineau-Des-
FIGURE 20.?Rostrum of the Miocene flamingo Phoenicopterus
croizeti, drawn from a cast of a specimen in the Naturhisto-
risches Museum, Basel. The curvature is less than in adults
of modern species of Phoenicopterus but is similar to that seen
in their earlier developmental stages (see Figure 38c). (Scale
= 3.5 cm.)
voidy, 1863 (Insecta), all antedate Gervaisia Har-
rison and Walker, 1976a, and he therefore pro-
posed the name Harrisonavis as a substitute. The
distinguishing feature of the supposed new genus
was said by Harrison and Walker to be the less
bent bill with a broader tip. Figure 20 illustrates
a nearly complete rostrum of P. croizeti and shows
the less bent nature of the bill, the shallower keel,
and the broader tip, all of which occur in the
developmental stages of modern Phoenicopterus (see
Figure 38t). Thus P. croizeti does not possess char-
acters of generic significance as compared to ex-
tant taxa, the morphology of the bill being pre-
cisely what would be expected in an earlier, some-
what more primitive form of Phoenicopterus. We
regard Gervaisia Harrison and Walker, 1976a, and
Harrisonavis Kashin, 1978, as junior synonyms of
Phoenicopterus Linnaeus, 1758.
From Australia, A. H. Miller (1963) described
two flamingos of roughly the same age as Palae-
lodus and Phoenicopterus croizeti. One of these was
referred to a modern genus as Phoenicopterus novae-
hollandiae, and the other was described in a new
genus as Phoeniconotius eyrensis. The latter was
based on the distal end of a tarsometatarsus and
two phalanges and was characterized as being
more massive and less specialized for swimming
than modern flamingos. All fossil flamingos sub-
sequent to the early Miocene (except a few spec-
imens of Megapaloelodus) have been referred to
modern genera.
NUMBER 316 47
The fossil record of flamingos hitherto known
can be summarized as follows. None of the Me-
sozoic and early Tertiary fossils said to represent
flamingos have been identified with certainty and
for the present they may be discounted. In the
late Oligocene or early Miocene of Europe occurs
a species in the modern genus Phoenicopterus hav-
ing a somewhat more primitive bill structure than
recent forms. Contemporaneously, there was a
radiation of shorter-legged flamingos (Palaelodus
and Megapaloelodus), apparently more specialized
for swimming. At least one species of these per-
sisted until the early Pliocene. None of these
fossils gives any better clue to the ancestry of
flamingos than do the modern forms themselves.
To the foregoing may now be added a new
genus and species of middle Eocene flamingo.
This is the earliest certain member of the Phoen-
icopteridae and is based on a meaningful repre-
sentation of the skeleton. It is particularly signifi-
cant in showing an even closer approach to the
Charadriiformes than do recent flamingos.
A New Stilt-like Flamingo
from the Middle Eocene of Wyoming
Among the many fossil birds that had been
submitted to the late Alexander Wetmore for
study and which had remained unidentified, was
a small series of bones from a single locality in
the middle Eocene Bridger Formation of Wyo-
ming. These were collected in 1946 and 1947 by
C. Lewis Gazin, Franklin L. Pearce, and G. F.
Sternberg. According to Pearce's recollection, the
fossil birds at this locality all came from the same
level and from a relatively small area, although
no specimens were found in association.
Other than a single, undiagnostic distal end of
a femur of a yet unidentified larger bird (USNM
244323), apparently found somewhat apart from
the other specimens, all of the avian fossils from
FIGURE 21.?Bones of very young individuals referred to
Juncitarsus gracillimus: a, two portions of tibiotarsi: b, distal
end of tarsometatarsus. These probably indicate the presence
of a breeding colony. (Scale = 1 cm.)
48 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
this site appear to be from a single species. At
least three adults or sub-adults are represented,
along with several bones, possibly from a single
juvenile individual (Figure 21) that was almost
certainly too young to fly at the time of death,
thus suggesting the possibility of a breeding ag-
gregation. The individuals vary in size (Figure
22), perhaps indicating that the species was sex-
ually dimorphic.
This species was intermediate in size between
the larger extant Charadrii and the smallest ex-
tant flamingos. Its osteology shows a mosaic of
characters of both groups, but its presumably
derived features are those of flamingos, thereby
providing the earliest definite record of the
Phoenicopteridae. In the following descriptions
we have included some comparisons with Pres-
byornis (Presbyornithidae) in order to facilitate
identification of specimens in the event that ad-
ditional material comes to light.
Order CHARADRII FORMES Huxley, 1867
Suborder CHARADRII Huxley, 1867
Family PHOENICOPTERIDAE Bonaparte, 1831
Juncitarsus, new genus
TYPE-SPECIES.?Juncitarsus gracillimus, new spe-
cies.
DIAGNOSIS.?Referable to the Phoenicopteridae
by having the humerus with a single pneumatic
foramen, a distinct oval scar for M. scapulo-
humeralis cranialis, and the ectepicondylar spur
lacking; cervical vertebrae modified similarly to
modern Phoenicopteridae; intercotylar knob of
tarsometatarsus high and broad. Tarsometatarsus
extremely long and slender, most similar to Hi-
mantopus (Recurvirostridae); proximal end of hy-
potarsus level with cotylae; hypotarsus complex,
with closed canals; scar for hallux present; distal
foramen large and elongate; inner trochlea mark-
edly retracted posteriorly, with distinct wing; pos-
teroproximal border of middle trochlea truncate.
Attachment for anterior articular ligament of
FIGURE 22.?Anterior view of proximal ends of three tarso-
metatarsi of Juncitarsus gracillimus showing variation in size.
(Natural size.)
humerus sloping steeply. Thoracic vertebrae not
fused into a notorium.
ETYMOLOGY.?Latin juncus (a reed or rush) plus
tarsus, latinized from Greek tarsos (ankle), in ref-
erence to the extremely slender tarsometatarsus;
the generic name is masculine.
Juncitarsus gracillimus, new species
FIGURES 23,24b,25-27a, 28-31
HOLOTYPE.?Left tarsometatarsus lacking only
a portion of the anterior part of the proximal
end; hypotarsus slightly abraded. Vertebrate pa-
leontological collections of the National Museum
of Natural History, USNM 244318 (Figures 23,
25, 26/>,c); collected in 1947 by C. Lewis Gazin
(original number 140-47).
TYPE-LOCALITY.?Wyoming, Sweet water
County, "low buttes to extreme NE of Twin
Buttes and within Bridger" (C. L. Gazin, 1946
field catalog), in "yellow layer near base of buttes,
beneath a hard grayish green sandstone" (C. L.
NUMBER 316 49
B D
FIGURE 23.?Holotype, left tarsometatarsus of Juneitarsus gra-
cillimus (USNM 244318): a, anterior view; b, posterior view;
c, lateral view; d, medial view. (Natural size.)
Gazin, 1947 field catalog). Although Gazin (pers.
comm.) indicated that these buttes were those
indicated in the SE corner of section 33, T15N,
R109W (Buckboard Quadrangle, U.S. Geological
Survey 15 minute series topographic map, 1966),
successive searches of this locality in 1976, 1977,
and 1978 by Arnold D. Lewis, R. J. Emry, and
Olson, disclosed no vertebrate fossils other than
a few turtles. We later found that Gazin's 1946
field catalog refers to the locality as "near 1/4
section 22/27 corner," which would place it
slightly farther to the north (McKinnon Junction
Quadrangle); outcrops fitting the above descrip-
tions were located here in 1979 by Olson and
Lewis, but no additional bird remains were found.
HORIZON.?Middle Eocene, Bridger Forma-
tion. The site is very low in the Bridger, hence
the specimens are earliest middle Eocene in age.
ETYMOLOGY.?Latin gracillimus (very slender).
PARATYPES.?Proximal two-fifths of right tar-
sometatarsus lacking hypotarsus and not com-
pletely ossified, USNM 244319 (Figure 26a);
proximal two-thirds of right tarsometatarsus with
associated fragments of inner and outer trochleae,
USNM 244322; distal end of right tarsometatar-
sus of a very young individual, USNM 244327;
left tibiotarsus of very young individual lacking
tarsals and with proximal end unossified, USNM
244334; distal end of right tibiotarsus of juvenile
lacking tarsals, USNM 244337; abraded distal
end of right femur, USNM 244320; pedal pha-
lanx 1 of right digit II, USNM 244329; distal
two-thirds of pedal phalanx, USNM 244335;
worn proximal half of left humerus, USNM
244325 (Figure 27a); distal end of left humerus,
USNM 244330 (Figure 286); proximal fourth of
left ulna, USNM 244326 (Figure 28a1); portion of
a shaft of an ulna, USNM 244324; left radiale,
USNM 244333 (Figure 28c); anterior two-thirds
of left scapula of a juvenile, USNM 244328 (Fig-
ure 28a); unfused frontal bone of a juvenile,
USNM 244336 (Figure 31); anterior half of cer-
vical vertebra similar to the 6th cervical of Phoen-
icopterus, USNM 244338 (Figure 30a,b)\ cervical
vertebra similar to the 16th of Phoeni cop terns,
USNM 244321 (Figure 29); thoracic vertebrae
50 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
possibly equivalent to the 17th and 18th verte-
brae of Recurvirostra, USNM 244332 and 244331
(Figure 30c). All from the same locality and ho-
rizon as the holotype; C. L. Gazin field numbers
40-46, 139-47, 141-47, and 142-47.
MEASUREMENTS (in mm).?Holotype: Total
length 182, depth through hypotarsus about 12,
greatest proximal width about 10.5, least width
of shaft 3.8, least depth of shaft 4.0, width of shaft
at midpoint 3.9, depth of shaft at midpoint 5.1,
greatest width through trochleae 10.6, greatest
depth through trochleae 11.9, width of middle
trochlea 3.9, depth of middle trochlea 6.0, depth
through inner trochlea 6.3, depth through outer
trochlea 6.7.
Paratypes: Tarsometatarsus USNM 244322,
proximal width 9.6; ulna USNM 244326, proxi-
mal depth 9.7, proximal width 6.7, distance from
tip of olecranon to distal extent of attachment of
anterior articular ligament 8.3; humerus USNM
244325, distance from head to distal end of pec-
toralis attachment 24.5, length of scar for M.
scapulohumeralis cranialis 4.0; humerus USNM
244330, distal width 13.2, depth through external
condyle 7.4, diagonal length of external condyle
6.1 (humerus length estimated at 100); radiale
USNM 244333, greatest diameter 7.6; pedal pha-
lanx 1 digit II USNM 244329, length 19.1; tho-
racic vertebra USNM 244331, length of centrum
10.3; cervical vertebra USNM 244321, length
through centrum 14.4.
DIAGNOSIS.?As for the genus. Smaller than
any other known species of Phoenicopteridae;
larger than any member of the Recurvirostridae.
DESCRIPTION.?Tarsometatarsus: The extraor-
dinary tarsometatarsus of this species is somewhat
smaller than that of the smallest living flamingo,
Phoemconaias minor, but is much more slender (Fig-
ure 24), its proportions being approached among
recent birds only by the stilts {Himantopus; Recur-
virostridae). This element, in fact, is so nearly
identical in morphological details to that of Hi-
mantopus, that without the associated material it
would probably have been referred to the Recur-
virostridae, and within that family would have
been regarded as a close relative of Himantopus.
Only in the following details can the tarsometa-
tarsus of Juncitarsus be distinguished from that of
Himantopus: larger size; distal foramen larger and
more elongate (Figure 25d,e); middle trochlea
without the slight lateral deflection of Himantopus
but identical to Recurvirostra, distinct, small scar
for hallux (Figure 2be) (hallux lacking in Himan-
topus); wing of outer trochlea narrower and
slightly more produced posteriorly (Figure 25/);
attachment for M. tibialis cranialis more distinct
and elongate (Figure 25a); intercotylar knob
markedly higher and broader (Figure 26a). The
last feature is the only salient character separating
the tarsometatarsus of Juncitarsus from that of the
Recurvirostridae and the only one that shows a
closer approach to a condition in modern fla-
mingos.
The tarsometatarsus of Juncitarsus can be distin-
guished from that of modern flamingos by the
following features: outer trochlea narrower, with
wing in lateral view more perpendicular to the
shaft, not angling distally (Figure 25/); distal
foramen larger and more elongate; proximal bor-
der of posterior face of middle trochlea truncate
(Figure 25<?), not tapering proximally to form a
distinct V as in modern flamingos, but exactly
duplicating the condition in Recurvirostra; inner
trochlea rotated farther medially, giving the distal
end of the bone a narrower aspect than in modern
flamingos (Figure 24), and in medial view with a
wing distinctly set off from the body of the tro-
chlea (Figure 25c), as in recurvirostrids; hypotar-
sus more complex (Figures 2bb, 26b), with closed
canals matching Himantopus, not consisting of two
high calcaneal ridges with no canals as in modern
flamingos; hypotarsal block in proximal view
(Figure 26b) more pedicilate and in lateral view
(Figure 23c) at nearly the same level as the cotylae
(also true of Palaelodus), not set well below the
cotylae as in modern flamingos; base of hypotar-
sus extending distally as a ridge on shaft (Figure
FIGURE 24.?Anterior view of left tarsometatarsus: (a) stilt,
Himantopus mexicanus (Recurvirostridae); (b) Juncitarsus gracil-
limus (Phoenicopteridae; reconstructed from two specimens);
(c) flamingo, Phoeniconaias minor (Phoenicopteridae); (d) stork,
Ciconia abdimii (Ciconiidae). (Scales = 1 cm.)
NUMBER 316 51
II
I)
S; ]
ill
?" v
52 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
NUMBER 316 53
FIGURE 25.?Details of holotype tarsometatarsus of Juncitarsus
gracillimus (USNM 244318): a, proximal end, anterior view;
b, proximal end, posterior view; c, distal end, medial view;
d, distal end, anterior view; e, distal end, posterior view;
/ , distal end, lateral view. (Specimen coated with ammonium
chloride; X 3.)
25b), much more pronounced than in modern
flamingos but similar to Himantopus.
The tarsometatarsus of Juncitarsus is more slen-
der and elongate than in either Presbyornis or
Palaelodus. In Palaelodus (Figure \9b) the shaft is
much deeper and more laterally compressed, the
hypotarsus more complex, the proximal end pro-
portionately wider, the intercotylar knob heavier,
FIGURE 26.?Tarsometatarsi of Juncitarsus gracillimus: a, prox-
imal end in anterior view, paratype of subadult (USNM
244319) to show development of intercotylar knob; b, holo-
type (USNM 244318), proximal view; c, same, distal view.
( X I )
the inner trochlea much deeper and more
rounded, and in posterior view more elongate. In
Presbyornis, the hypotarsus is much wider basally,
has no closed canals, the inner calcaneal ridge is
reduced and the outer one produced distally as a
hook; the distal end of the tarsometatarsus differs
from that of Juncitarsus in that the inner trochlea
is less retracted posteriorly and lacks a distinct
wing; the middle trochlea is more elongate and
not truncate on the posterior face, and the outer
trochlea is deeper. The tarsometatarsus of Junci-
tarsus bears no resemblance to that of any member
of the Ciconiiformes (e.g., Figure 24).
Humerus: The two portions of humerus of Jun-
citarsus, unlike the tarsometatarsus, bear no resem-
blance to the humerus in recurvirostrids. The
proximal end (Figure 27a) appears to have been
pneumatic (a small portion of the border of the
pneumatic foramen remains in the one specimen)
and does not have the deeply excavated,
nonpneumatic tricipital fossae that are character-
istic of the Recurvirostridae, most other Charad-
riiformes, and Presbyornis. In the distal end, the
distinct ectepicondylar spur characteristic of re-
curvirostrids and most other shorebirds is absent,
as in flamingos.
?ft
FIGURE 27.?Proximal ends of left humeri of fossil flamingos:
a, Juncitarsus gracillimus (USNM 244325); b, Palaelodus sp.
(Scales = 1 cm).
54 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
The most characteristic feature of the proximal
end of the humerus in Juncitarsus is a distinct
elliptical scar for M. scapulohumeralis cranialis
(the "supraspinatus" scar of Howard, 1929), dis-
tal to the pneumatic foramen and lying between
that opening and the midline of the shaft. A
similar deep scar is characteristic also of Palaelodus
(Figure 21b) and may be faintly seen in those
individuals of modern flamingos in which the
pneumatic foramen is less extensive and does not
obliterate this area. We regard the resemblance
of this scar in Juncitarsus, Palaelodus, and modern
flamingos as significant, as we have not seen a
similar condition in any modern group of birds,
including the Ciconiiformes, Anseriformes, or
Charadriiformes. The overall configuration and
details of the proximal end and shaft of the
humerus in Juncitarsus very closely resemble that
in Palaelodus and modern flamingos. In all of these
forms, the margin of the deltoid crest describes a
long, gentle curve extending well down the shaft,
in contrast to that seen in Ciconiiformes, in which
the deltoid crest is variable but always shorter
and more angular, as, for example, in storks and
herons. Likewise, in Juncitarsus, Palaelodus, and
modern flamingos, the scar of M. latissimus dorsi
pars cranialis is quite similar, being situated mid-
way between the midline and the external margin
of the shaft, whereas in Ciconiiformes this scar is
either on the midline or lies between it and the
internal margin of the shaft.
The single distal end of humerus available for
Juncitarsus (Figure 286) has the anconal surface
and the area of the brachial depression crushed
FIGURE 28?Paratypes of Juncitarsus graallimus: a, left scapula, dorsal view (USNM 244328);
b, distal end of left humerus, palmar view (USNM 244330); c, left radiale, proximal view
(USNM 244333); d, left ulna, internal view (USNM 244326). (X 3.)
NUMBER 316 55
and is therefore not particularly useful. One dis-
tinctive feature is the raised internal margin and
steeply angled surface of the attachment of the
anterior articular ligament. From Presbyornis it
differs further in having the internal condyle in
distal and palmar views more rounded and the
external condyle relatively narrower. Palaelodus
and modern flamingos differ from Juncitarsus in
having the external condyle curved internally at
the proximal tip.
Ulna: The proximal end of an ulna of Junci-
tarsus (Figure 28d) is generally similar to that in
modern flamingos, but the attachment of the
anterior articular ligament is broadly triangular
and does not extend distally along the impression
of M. brachialis. In this respect Juncitarsus more
nearly resembles the Recurvirostridae and differs
greatly from Palaelodus?in which the attachment
of the anterior articular ligament is very narrow
and elongate. The proximal radial depression in
Juncitarsus is deeper than in the forms just men-
tioned.
Radiale: A well-preserved left radiale (Figure
28c) is generally similar to that of modern fla-
mingos, although we have not made extensive
comparisons of this element. It agrees with fla-
mingos, as opposed to recurvirostrids, in being
more elongate and in having a distinct notch in
the dorsal surface. It is proportionately narrower
than in modern flamingos, but otherwise is more
similar to the Phoenicopteridae than to the Ci-
coniiformes or Charadriiformes.
Scapula: The only available scapula of Junci-
tarsus (Figure 28a) is the anterior portion from a
juvenile. The coracoidal articulation is perhaps
slightly better developed than in Phoenicopterus
but not as distinctly produced as in Palaelodus or
Presbyornis, nor a distinct ball as in storks and
herons. The acromion is not as elongate and
pointed as in Presbyornis, Palaelodus, or modern
flamingos, and is not unlike that of Himantopus.
The shaft is narrow, rather rounded in cross-
section, and deflected ventrally, as in Palaelodus,
Presbyornis, and modern flamingos, and quite un-
like the broad flattened condition in Ciconi-
iformes.
Vertebrae: We undertook comparisons of the
four vertebrae included among the material of
Juncitarsus with little anticipation of discovering
much of interest. We found, however, these spec-
imens were of great value in assessing the affinities
and adaptations of the bird.
The most complete specimen corresponds very
closely with the 16th cervical of Phoenicopterus
(15th of Phoeniconaias), differing mainly in the
narrower and longer prezygapophyses and the
narrower and deeper articular surfaces of the
centrum. In modern flamingos, this vertebra oc-
curs at the point of transition from the greatly
elongated anterior cervicals to the shortened pre-
thoracic cervicals. It is characterized by having
the ventral surface of the centrum elongate and
flat, with two distinct anterior hemapophyses,
and by having a large, sloping, expanded neural
crest. The agreement of the fossil with modern
flamingos is striking (Figure 29), particularly
since we found no vertebra comparable in pro-
portions and details in any of the other orders of
birds possibly related to flamingos, including the
Charadriiformes. In the Recurvirostridae the
equivalent vertebra is much shorter, has no neural
crest, and has only a single hemapophysis. In the
Anatidae, the vertebrae in this area are somewhat
similar but are not as elongate and do not possess
a combination of a high neural crest and double
hemapophyses. The transitional cervical verte-
brae in the families of Ciconiiformes are not as
well demarcated, except in herons. There is con-
siderable difference between the families, but
none approaches the condition in flamingos. In
herons, for example, the ventral surface of the
most nearly comparable vertebra bears a large,
thin crest, totally unlike the double hemapo-
physes and flattened and elongated centrum of
modern flamingos and Juncitarsus.
A fragmentary anterior portion of an anterior
cervical of Juncitarsus (Figure 30a,b) indicates a
very elongate and slender vertebra with a dis-
tinctly oval cross-section (Figure 30a) such as seen
in modern flamingos. It is most similar to the 6th
cervical in Phoenicopterus, differing in having the
hemal spines reduced and more widely divergent
56 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
NUMBER 316 57
FIGURE 29?Cervical vertebra of Juncitarsus gracillimus (para-
type USNM 244321) compared with the 15th cervical ver-
tebra of the modern flamingo Phoemconaias minor (primed
letters): a, lateral view; b, dorsal view; c, ventral view;
d, anterior view; e, posterior view of centrum. (Juncitarsus X
2.6; Phoemconaias X 2).
and the ventral surface of the centrum forming a
slight crest rather than being flattened; in the last
feature it is like Himantopus. Only the Ardeidae
have comparably elongated vertebrae. The fossil
agrees with flamingos and differs from herons in
the deeper anterior articular surface and the shal-
lower depression on the ventral surface posterior
to the articulation.
Another vertebra of Juncitarsus (Figure 30c)
bears a costal facet and therefore formed part of
FIGURE 30.?Paratypical vertebrae of Juncitarsus gracillimus:
a, anterior cervical equivalent to 6th cervical vertebra of
Phoenicopterus, cross section (USNM 244338); b, same, lateral
view of right side; c, thoracic vertebrae equivalent to the
17th and 18th vertebrae of Recurvirostra, lateral view of left
side (USNM 244332, 244331). (X 3.)
the thoracic series. It bears the remains of a single
large hemal spine and thus came from the ante-
rior portion of the series. In modern flamingos
these vertebrae are fused into a notorium and the
neural spines are less prominent. The present
vertebra had a large neural spine and was un-
fused. It bears no resemblance to any of the
thoracic vertebrae of modern flamingos but
agrees very closely with the 17th vertebra (2nd
thoracic) of Recurvirostra.
A second specimen of thoracic vertebra (Figure
30c) was also unfused and bears a costal facet.
The centrum is laterally compressed unlike mod-
ern flamingos. This vertebra also agrees well with
Recurvirostra and appears to be the one succeeding
the previously mentioned thoracic.
The resemblance of the thoracic vertebrae of
Juncitarsus is closest to the Charadriiformes. As
with the cervicals, there is great variation in the
thoracic vertebrae between the families of Cico-
niiformes, none of which have the centra as com-
pressed as in Juncitarsus. In storks and herons none
of the thoracics bear well-developed hemal spines.
In ibises some of the thoracics are fused into a
notorium, but this involves a different series of
vertebrae than that of modern flamingos.
Frontal Bone: Associated with the other mate-
rial of Juncitarsus is a small unfused frontal bone,
the sutures of which obviously had not closed. It
is important in showing in the supraorbital area
a distinct impression for a salt gland (Figure 31),
in the same position as seen in modern flamingos.
Pedal Phalanx: A toe bone appears to be pha-
lanx 1 of right digit II. The element differs from
modern flamingos in being less laterally com-
pressed, and from storks and herons in being less
elongate. Its resemblances are closer to the Re-
curvirostridae.
Femur: An abraded distal end of a femur re-
ferred to Juncitarsus preserves no useful characters.
DISCUSSION.?Juncitarsus is the earliest known
fossil that is definitely referrable to the Phoeni-
copteridae. It is known as yet only from the
earliest Middle Eocene. Presbyornis, a colonial
charadriiform near the ancestry of Anseriformes,
is abundant in early Eocene deposits and thus
58 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 31.?Unfused frontal bone of juvenile specimen of
Juncitarsus gracilUmus (USNM 244336) showing depression for
salt gland (arrow). (X 3.)
must have been contemporaneous with the ances-
tors of Juncitarsus.
The available evidence indicates that Juncitar-
sus may have nested colonially. It had salt excret-
ing glands and therefore inhibited saline environ-
ments at least intermittently, if not entirely. Both
of these conditions are typical of modern flamin-
gos.
Juncitarsus possessed apparently derived char-
acters of the cervical vertebrae and humerus
which ally it with the Phoenicopteridae, although
it retains the morphology of the Charadriiformes
in the thoracic vertebrae and most features of the
tarsometatarsus. The last element is particularly
similar to that of the Recurvirostridae, corrobor-
ating our proposed relationship between the
Phoenicopteridae and the Recurvirostridae. That
the cervical vertebrae of Juncitarsus are specialized
like those of modern flamingos suggests that some
of the aspects of the highly modified feeding
apparatus of flamingos had evolved by the Mid-
dle Eocene. The thoracic vertebrae of Juncitarsus
are unfused, indicating that the notorium of mod-
ern flamingos evolved subsequent to the special-
izations of the neck.
Juncitarsus provides a mosaic of phoenicopterid
and charadriiform characters and in size bridges
the gap between the modern members of the
Recurvirostridae and the Phoenicopteridae. It
shows no approach to the morphology of either
Ciconiiformes or Anseriformes.
Aspects of Evolution of Filter Feeding
The most characteristic feature of flamingos is
their filter-feeding apparatus, which has been
likened to that of the Anseriformes and therefore
has been cited as evidence for a relationship
between the two groups. Greatly detailed descrip-
tions of the structure and function of the feeding
apparatus are available for flamingos (Jenkin,
1957) and for ducks (Goodman and Fisher, 1962;
Zweers, 1974; Zweers et al., 1977). These lack,
however, a more general overview of evolutionary
events that may have led to development of such
adaptations.
Filter feeding is commonly employed in diverse
groups of invertebrates and in some fishes and
tadpoles. Among higher vertebrates, however,
well-developed straining devices have evolved
only in baleen whales and in three groups of
birds: flamingos, ducks, and one genus of petrels
{Pachyptila, Procellariidae). Certain penguins
(Spheniscidae) and auks (Alcidae) show some of
the structures needed for feeding on small orga-
nisms but have not evolved lamellate strainers. It
is instructive to examine their adaptations first.
Zusi (1974a) has provided a valuable account of
feeding adaptations in penguins, and Bedard
(1969) has discussed those of alcids. The plank-
ton-eating forms of these groups are characterized
by an enlarged tongue, a broadened rostrum, and
cornified papillae on the roof of the mouth and,
in the case of penguins, on the tongue, inner
surface of lower jaw, and larynx also. The en-
larged tongue may be accomodated in two ways;
either by a distensible gular pouch as in alcids, or
by a deepening of the bones of the lower jaw, best
exemplified in penguins by species of the genus
Eudyptes. The penguins and alcids thus adapted,
feed largely on small crustaceans which are
thought to be taken individually rather than with
a netlike scooping (Zusi, 1974a: 76). Prey is taken
very rapidly, however, and is held and manipu-
lated toward the throat by action of the tongue.
The next steps in the evolution of filter feeding
are well illustrated by the petrels of the genus
Pachyptila, sometimes known as whalebirds, on
account of the baleen-like feeding apparatus in
NUMBER 316 59
some species. In Pachyptila there is a continuum
of variation in bill shape, from proportions nearly
typical of other members of the family (P. belcheri)
to the grotesquely broadened bill of P. vittata (see
illustrations in Murphy, 1936; Fleming, 1941).
All have an enlarged tongue, which, as with the
plankton-feeding alcids, is accomodated by a dis-
tensible gular pouch rather than by a deep lower
jaw. Each possesses at least the rudiments of
lamellae, always on the inner surface of the edge
of the upper jaw, with more pronounced devel-
opment posteriorly than anteriorly. In the nar-
row-billed species these "lamellae" are very small
transverse projections extending medially less
than a millimeter from the cutting edge of the
bill. They reach their extreme in P. vittata, which
possesses a bona fide straining device consisting
of a series of plate-like lamellae extending ven-
trally some 3.5 mm from a ridge inside the edge
of the bill.
Although Murphy (1936:614) held that in the
narrow-billed forms of Pachyptila "it would be
hard to believe that the faint striations [in the
upper jaw] could have any function whatsoever,"
it is more difficult to believe that such structures
would evolve without having some function.
Quite probably the rudimentary lamellae in the
less specialized filter-feeding petrels provide gaps
for the expulsion of water while the prey is held
in place with the tongue. With increasing spe-
cialization, the lamellae enlarge and begin to
assume the role of food retention while the tongue
forces out water and moves the prey toward the
throat. As with penguins (Zusi, 1974a) and fla-
mingos (Jenkin, 1957), increasing specialization
of the feeding apparatus in Pachyptila is correlated
with a decrease in size of prey (Watson, 1975).
The filter-feeding petrels thus illustrate several
important points. First, the initial adaptation for
filter-feeding is enlargement of the tongue. This
is accompanied or followed by widening and
deepening of the bill and the development of
lamellae. Secondly, the initial function of lamel-
lae may be to permit the expulsion of water rather
than to retain prey. Third, the species of Pachyptila
show progression from a primitive, nearly unmod-
ified species, to a highly evolved lamellate filter
feeder within a single extant genus, suggesting
that the great broadening of the bill and the
development of a fine strainer may occur rapidly
in birds. Fleming (1941) considered speciation in
Pachyptila to be the result of climatic changes
associated with Pleistocene glacial events, which,
if true, would make the more specialized filter-
feeding adaptations in the genus of very recent
origin.
Flamingos are the most specialized of avian
filter feeders. The peculiarly bent bill, used in an
"upside down" attitude when feeding, separates
the living flamingos from all known birds. Two
strikingly different modifications of the bill occur
in flamingos, the least specialized being that of
Phoenicopterus, the most derived condition being
that found in Phoenicoparrus and Phoeniconaias. In
all flamingos the lower jaw is deep and swollen
and the upper jaw is narrow. In Phoenicopterus
(Figure 32), the lower jaw is essentially a large
cylinder housing an immense tongue equipped
with a series of spiny protuberances. Fine ridges
lying transverse to the long axis of the bill occur
on the narrow dorsal surface of the two sides of
the lower jaw. The upper jaw is rather flat, with
a slightly developed median keel. Coarse hooklike
lamellae are present on the outer edge of the
upper jaw, inside of which is a series of diagonally-
oriented, fine plate-like lamellae lying in a narrow
band between the outer edge of the jaw and the
bare median keel.
In Phoenicoparrus and Phoeniconaias the upper
jaw is much narrower and bears a deep median
keel (Figure 39a), with long rows of exceedingly
fine microscopic, feather-like lamellae. The coarse
lamellae along the edge of the jaw are much finer
and less hooklike than in Phoenicopterus. In the
lower jaw, the space for the tongue is greatly
reduced because the dorsal lamellate ridges seen
in Phoenicopterus have expanded and are turned
inward and downward to provide a greater sur-
face area for rows of fine lamellae opposing those
of the keel on the upper jaw. Phoeniconaias feeds
on much smaller food particles than does Phoeni-
copterus (Jenkin, 1957).
The filtering apparatus in the Anatidae is quite
different from that of flamingos but the essential
60 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 32.?Head of the flamingo Phoemcopterus ruber. Lower
jaw removed and displaced below, viewed from the external
surface. Note that the tongue is housed in the lower jaw and
that neither the lower jaw nor the keel on the upper jaw are
as deep as in Phoeniconaias (see Figure 39).
FIGURE 33.?Head of a Mallard Duck, Anas platyrhynchos.
Upper jaw removed and displaced above, viewed from the
internal surface and reversed to preserve the same orienta-
tion. Note that the tongue is accomodated by the upper jaw
and that there are two bulges in the tongue that form a
double piston suction pump, unlike the mechanism in the
flamingo.
structures are all present: enlarged tongue, broad
bill, and lamellae. The bill shape of ducks is too
familiar to need description but perhaps it has
not been realized that it presents an adaptation
not found in other filter-feeding vertebrates: the
enlarged tongue is accomodated by the upper
rather than the lower jaw (Figure 33). This is a
fundamental difference between ducks and fla-
mingos and one that has not been emphasized by
those attempting to ally the two groups. Further-
more, the underlying bony structure of the tongue
is very different in the two groups. In ducks, the
paraglossale, the terminal bone of the hyoid ap-
paratus supporting the tongue, is a distinctive
expanded, spatulate bone, whereas in flamingos
it is slender and more rodlike, as is typical of most
birds.
In typical anatids, rows of lamellae lie along
the inner surfaces of both the upper and lower
jaws, the latter series being divided into upper
and lower rows. The morphology of these lamel-
lae may vary considerably, even within a genus.
In Anas, the lamellae may be coarse, hard plates,
as in the Mallard Anas platyrhynchos, or they may
be prolonged into fine hairlike fringes as in the
congeneric Shoveler Anas clypeata. Again, as in
Pachyptila, the evolution of fine lamellate struc-
tures seems to be accomplished with relative ease.
In no case, however, are the lamellae in ducks like
the rows of platelets or feather-like strainers of
flamingos.
The process of filtration in flamingos is quite
different from that of ducks. In flamingos, the
mouth is opened and water enters along the entire
gape, which then closes, the tongue forcing water
back through the filtering devices. In the normal
feeding process of Phoeniconaias and when Phoeni-
copterus feeds on mud, this process is modified so
that the outer lamellae function as excluders,
keeping out larger inorganic particles (Jenkin,
1957). In ducks, the bill and tongue act as a
suction pressure pump consisting of two pistons
in a cylinder (Figure 33), with the water entering
at the tip of the bill and being expelled posteriorly
(Zweers et al., 1977).
The advocates of ciconiiform relationships of
flamingos have not hypothesized how the com-
plicated filter-feeding apparatus might have
evolved from the hard, pointed bill of a stork;
indeed it is difficult to envision such a transfor-
mation taking place. Several authors (Reichenow,
1877; Jenkin, 1957; Sibley et al., 1969) have
NUMBER 316 61
FIGURE 34.?Bills of two specimens of the African Open-bill Stork, Anastomus lamelligerus, to
show the variation in development of the bristly pads on the ramphotheca. It is obvious by
their placement that these structures could have no filtering function.
mentioned the so-called "lamellae" of the open-
bill storks, Anastomus, in connection with the
evolution of straining devices in flamingos, but
the analogy is invalid. The structures on the
rhamphothecae of Anastomus (Figure 34) are in no
way comparable to lamellae. Kahl (1971:27)
much more appropriately refers to them as
"leathery columnar 'pads.'" He has shown that
the open-bill structure in Anastomus provides a
forceps-like action of the bill tips that functions
in preying on mollusks, particularly large snails,
which are the chief item of diet in these storks.
The bristly pads on the rhamphothecae of
Anastomus probably do not function in feeding.
They occur along the edges of the gap in the bill
and their relative prominence appears to be cor-
related with the age of the individual, as there is
considerable variation in development (Figure
34). In most birds, the edges of the upper and
lower jaws come in contact, serving to keep the
horny rhamphothecae worn down and probably
sharpened as well (Tunnicliffe, 1973). Such con-
tact is not possible in Anastomus, however, and the
rhamphothecae appear to be unable to check
each other against continued outgrowth. Thus
the bristly pads in this genus may well be purely
adventitious structures. Regardless, Anastomus
does not represent any stage in the evolution of
filter feeding.
Because we propose a shorebird ancestry both
for flamingos and for ducks (Olson and Feduccia,
in press), there should be taxa among the Char-
adriiformes having morphological precursors of
phoenicopterid and anatid feeding adaptations.
Within the Recurvirostridae, Recurvirostra and
Cladorhynchus are adapted for feeding rapidly on
large numbers of small prey items. Accordingly,
the tongue is enlarged and is short, broad, and
62 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
fleshy (Figure 35), to facilitate movement of small
prey into the throat. The development of a large,
fleshy tongue, as we have noted, is the first major
step involved in the evolution of filter feeding. In
storks, however, the tongue is rudimentary (Gard-
ner, 1925).
An unrecognized example of a shorebird show-
ing the beginning stages in the development of
filter feeding is the Red Phalarope, Phalaropus
fulicarius (Phalaropodidae). In the other two mem-
bers of the Phalaropodidae (Lobipes lobatus and
Steganopus tricolor) the bill is extremely slender,
pointed, and needlelike (Figure 36/>), but in Phal-
aropus the bill is broad, deep, and subspatulate in
shape (Figures 36a, 376, 38a), with wide, flexible
margins. The tongue is correspondingly enlarged
and from the postero-lingual rims of the lower
jaw project a few well-developed, narrow papillae
that may function as strainers (Figure 36a). In
other phalaropes the tongue is narrow and pa-
pillae in the lower jaw are absent or very rudi-
mentary (Figure 36?). Phalaropus fulicarius feeds
mainly on small insects and crustaceans and is
reported to take food at a much faster rate than
other phalaropes (Bent, 1927). Harold Mayfield
(in litt. to Olson, 17 January 1978) writes that on
the breeding grounds, Phalaropus may be seen to
feed by extracting chironomid midge larvae from
floating vegetation and often is observed with
strands of vegetation hanging from the mouth.
B
FIGURE 35.?Mouth of the American Avocet, Recurvirostra
ameruana, to show the broad, fleshy tongue. The acquisition
of such a tongue is the first step in the development of filter-
feeding.
FIGURE 36.?Dorsal view of the lower jaw and tongue of a
Red Phalarope, Phalaropus fulicarius (a), and a Northern
Phalarope, Lobipes lobatus (b). The broad bill, enlarged
tongue, and papillae of Phalaropus probably indicate a ca-
pacity for primitive filter-feeding.
He reports that stomachs almost always contain
bits of vegetation apparently taken in acciden-
tally while feeding. Thus it appears that Phalaro-
pus actually engages in a primitive straining type
of filter-feeding as would be predicted from its
morphology.
The bill in most Charadriiformes is typically
rather weak and flexible, due in large measure to
the long schizorhinal nostrils and the short pre-
maxillary and mandibular symphyses. This has
proved to be a very plastic structure, and conse-
quently the Charadriiformes exhibit the greatest
diversity in feeding adaptations of any order of
birds (see examples illustrated in Zusi, 1974b).
Contrast, for example, the bill of a Spoonbill
Sandpiper (Eurynorhynchus) with that of a skim-
mer (Rynchops).
NUMBER 316 63
It is well known that the bill in young flamingos
is straight and only later in ontogeny develops
the characteristic crook. This has received only
passing comment in the literature, with most
authors stating that the flamingo bill is "goose-
like" in its early stages. The bill in flamingos is
never really gooselike but in its earliest stages can
better be likened to that of a shorebird such as
Phalaropus, being rather long and narrow with
somewhat flexible margins (Figure 37). In lateral
view, the bill is deeper than usual for most Char-
adrii (Figure 38b) and ontogenetic changes in-
volve increasing the depth of the mandible and
the curvature of both jaws (Figure 38c,d). At one
point in the development of Phoenicopterus ruber,
the bill is shaped almost exactly as in the early
Miocene species P. croizeti (Figures 20, 38c), and
the ontogeny of the bill in modern flamingos
appears to reflect rather closely their phylogeny.
To evolve such a structure from the condition
typical of the Charadrii would mainly require
fusion by increased ossification of various separate
elements, whereas to evolve the flamingo feeding
apparatus from the already greatly fused cranial
structure of a stork would involve a series of
highly improbable intermediate stages.
\
B
FIGURE 37.?Dorsal view of bill of downy chick of a flamingo, Phoenicopterus ruber (a) compared
to an adult Red Phalarope, Phalaropus fulicarius (b).
64 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 38.?Lateral view of bill: a, Red Phalarope, Phalar-
opus fulicanus; b-d, progressive developmental stages of fla-
mingos: b, downy chick of Phoemcopterus ruber less than a week
old; c, chick of P. ruber about 30 days old; d, chick of
Phoemconaias minor 7 weeks old (adapted from Kear and
Duplaix-Hall, 1975, plate 48). Note the progressive deepen-
ing of the mandible and bending of the bill with increasing
age.
Although the filtering techniques of flamingos
and ducks are entirely different from one another,
both methods require repeated and rapid opening
of the bill, which can be accomplished by moving
either the upper or the lower jaw, or both. Be-
cause M. depressor mandibulae causes protrac-
tion of the upper jaw as well as depression of the
mandible (Zusi, 1967), it has a very important
role in the feeding process in flamingos and in
ducks. The enlarged bladelike retroarticular pro-
cesses of the mandible in both groups provide
increased area for the insertion of the depressor
mandibulae. The retroarticular processes and de-
pressor mandibulae are well-developed in several
groups of shorebirds, notably so in Recurvirostra
(Burton, 1974), and although not as exaggerated
as in flamingos and ducks, are quite suitable as
precursors. Such retroarticular processes are lack-
ing in storks and herons, however. Because of the
importance of the depressor mandibulae in filter-
feeding, regardless of how such filtering is accom-
plished, it is not improbable that the enlarged
retroarticular processes of flamingos arose inde-
pendently of those in ducks.
The astute naturalist Stejneger (1885:153)
noted in passing the resemblance between the
feeding apparatus of flamingos and that of baleen
whales, but devoted only a sentence to it. The
similarity between the head of a flamingo and
that of the right and bowhead whales (Eubalaena
and Balaena) is quite striking. In these whales the
upper jaw is quite narrow, with a ventral keel
bearing long plates of baleen. The lower jaw is
very deep and swollen, accomodating a huge
tongue and rising up so as to cover the baleen
plates of the upper jaw when the mouth is closed.
Unlike flamingos, there are no straining devices
on the lower jaw, but otherwise the general ap-
pearance of the head is so like that of flamingos
(Figure 39) as to be one of the more outstanding
examples of convergence in the animal kingdom.
The resemblances extend to the skeleton as
well. The rostrum in Eubalaena and Balaena, par-
ticularly as compared to that in other baleen
whales such as Balaenoptera, is markedly crooked
and bent downward so that it is superficially like
that of a flamingo (Figure 40). The bony structure
of the lower jaw is not like that of flamingos
because the great depth of the lower jaw in
Balaena is achieved by a mass of connective tissue
built up on a mandible not substantially different
from that of other baleen whales.
NUMBER 316 65
B
FIGURE 39.?Head of a Lesser Flamingo, Phoemconaias minor (a), compared with that of a Black
Right Whale, Eubalaena glaaalis (b), to show the convergent similarities in the filter-feeding
apparatus.
66 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
FIGURE 40.?Skull of a Lesser Flamingo, Phoemconaias minor
(a), compared with that of a Black Right Whale, Eubalaena
glaaalis (b), to show the similarity in the shape of the long,
decurved bony structure of the rostrum.
The bend in the rostrum of Balaena and in the
deep-keeled flamingos confers one obvious advan-
tage: it allows the filtering devices in the middle
portions of the rostrum to become much longer
and more extensive. Balaena has the longest and
finest baleen of any of the filter-feeding whales
and as a consequence feeds on smaller organisms.
The bent rostrum must confer other advan-
tages, however, for Phoenicopterus has no deep keel.
First of all, it provides space for an enlarged
tongue while still allowing the tips of the jaws to
come together, thereby permitting flamingos to
pick up individual food items (Rooth, 1965) and
to manipulate nesting material. More impor-
tantly, the bend in the bill also allows the entire
length of the gape to be opened with a minimum
of movement of the jaws (Jenkin, 1957). At least
in flamingos, the bend must first have arisen for
these purposes, being followed by its use for ex-
pansion of the filtering apparatus in the more
advanced species.
The similarity of the heads of flamingos and
whales is probably a good indication that the
bent structure of the flamingo bill arose in ac-
cordance with the constraints of filter feeding
alone, the "upside-down" feeding posture having
evolved secondarily. The more primitive baleen
whales, with their straighter and wider upper
jaws, might provide useful analogs to the mor-
phological stages through which flamingos may
have passed during their evolution, although this
is demonstrated just as well in the ontogeny of
living species (Figure 38).
Modern flamingos feed in highly saline waters
and the available evidence indicates that the
earliest fossil flamingo, Juncitarsus, may have oc-
curred in a similar habitat. The same is true of
Presbyornis, a filter-feeding charadriiform near the
ancestry of ducks. Highly saline lakes provide
abundant food in the form of swarms of brine-
adapted arthropods and growths of algae. The
small size of these organisms, however, would
necessitate a filtering device for effective feeding.
Furthermore, in such habitats there would be
strong selection for feeding methods that prevent
the ingestion of water, in order to avoid the higher
energetic cost of metabolic excretion of salt. Thus,
highly saline lakes may have been the original
habitat for both flamingos and Anseriformes.
There, selection would have favored the devel-
opment of specialized filtering mechanisms that
might never have evolved under less strenuous
conditions.
To summarize, the filter-feeding adaptations of
flamingos are seen to be entirely different from
those of the Anseriformes and are not indicative
of a relationship between these two groups. Mor-
phological precursors for such adaptations exist
among the Charadriiformes but not in storks.
Conclusions
The association of the Phoenicopteridae with
the Ciconiiformes has resulted solely from histor-
ical traditions and misconceptions. We have
shown that there is no substantial or convincing
evidence of relationship between flamingos and
either the Ciconiiformes or Anseriformes, whereas
all of the attributes of flamingos are compatible
with a charadriiform origin, including those that
once seemed inexplicable when flamingos were
considered as bewildering mosaics of ciconiiform
and anseriform characters.
If flamingos were derived from Ciconiiformes
NUMBER 316 67
and converged towards Charadriiformes, one
would expect fossil flamingos to have more stork-
like characters than modern flamingos (which
have no stork-like characters anyway). This is
definitely not the case, for the earliest known
flamingo, Juncitarsus, has no similarities to the
Ciconiiformes and in many respects is more sim-
ilar to the Recurvirostridae than are modern
flamingos. We cannot see that convergent evolu-
tion is really responsible for the confusion sur-
rounding the classification of flamingos; their
similarities to storks go no farther than the simi-
larities between all birds with long legs and long
necks.
The Anseriformes likewise prove unsatisfactory
as ancestors of flamingos. Although members of
both groups have webbed feet, swim and tip up
while feeding, and have honking vocalizations,
so, too, do members of the charadriiform family
Recurvirostridae. The fact that both flamingos
and ducks are filter feeders is of no systematic
consequence because their basic structural adap-
tations for filtering are completely dissimilar and
evolved independently of one another. Flamingos
and Anseriformes share similar mallophagan par-
asites, but new knowledge of the evolutionary
history of these two groups provides a logical
explanation for this that does not involve a close
relationship of the hosts: the ancestors of both
flamingos and ducks originally evolved in the
same harsh saline environments and probably
had similar breeding habits that would have
promoted transfer of parasites between the downy
young. No anatomical evidence exists that sup-
ports an ancestral-descendant relationship for
Anseriformes and flamingos.
On the other hand, in virtually all of their
features that are not unique, flamingos resemble
the Charadriiformes. This is supported by osteol-
ogy, myology, behavior, internal parasites, and
by the existence of a fossil form intermediate
between the Recurvirostridae and modern fla-
mingos.
In their prediliction for highly saline environ-
ments, their coloniality, simplified breeding dis-
plays, habit of feeding on very small prey, en-
larged fleshy tongue, and large retroarticular pro-
cesses of the mandible, the Recurvirostridae pos-
sess the necessary ecological, behavioral, and mor-
phological precursors of the more specialized fea-
tures of flamingos. Furthermore, modern fla-
mingos and the recurvirostrid Cladorhynchus share
certain characters that are either derived for all
birds (M. iliotibialis medialis; breeding habits) or
are derived within the Charadriiformes (two coats
of white, unpatterned nestling down; elongated
tertials). Cladorhynchus is nevertheless clearly a
member of the Recurvirostridae. Thus the evi-
dence suggests that flamingos evolved directly
from the Recurvirostridae rather than from a
proto-recurvirostrid. Otherwise, it would have to
be assumed either that all the derived characters
shared by Cladorhynchus and flamingos evolved
twice, which is implausible, or that all recurviros-
trids once possessed these characters and that
Recurvirostra and Himantopus have lost them and
"re-evolved" all their primitive, more typically
charadriiform characters, which is even less likely.
If flamingos evolved directly from the Recurvi-
rostridae, then it must be assumed that the Re-
curvirostridae were in existence before the middle
Eocene, when the first flamingos appear. As yet,
the only fossils possibly belonging to the Recur-
virostridae are a few fragmentary bones of Mio-
cene age.
The principal differences between modern fla-
mingos and the Recurvirostridae are in the highly
modified feeding apparatus, the increased num-
ber and specialization of the cervical vertebrae,
and the pneumaticity of the proximal end of the
humerus, with the associated changes in osteology
and myology of the shoulder. These characters
can then be said to define the family Phoenicop-
teridae. Although the nature of the feeding ap-
paratus is not known for the fossil genera Junci-
tarsus and Palaelodus, both taxa possess modified
humeri and cervical vertebrae and therefore are
clearly referable to the Phoenicopteridae.
Within the Phoenicopteridae there are three
basic generic groups: Juncitarsus, from the middle
Eocene; Palaelodus, from the late Oligocene or
early Miocene to early Pliocene; and "Recent"
68 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY
flamingos, from the late Oligocene or early Mio-
cene to the present. None of the known features
of the long-legged Juncitarsus would preclude it
from being very close to or on a direct line with
Recent flamingos, whereas the Palaelodus group
represents a separate, shorter-legged swimming
lin- ige. There is, as yet, no evidence to indicate
whether Palaelodus diverged from the more typical
flamingos before or after the evolution of Juncitar-
sus.
The Phoenicopteridae are shorebirds with a
highly evolved feeding apparatus. They are de-
rived not only from members of the suborder
Charadrii, but from a particular family of that
suborder, the Recurvirostridae. Their distinctive
peculiarities entitle them to rank as a separate
family, but it is not possible to accord them any
higher position, such as a suborder or order,
without raising each genus or family of Charad-
riiformes with a specialized feeding adaptation to
an equivalent rank?an obviously undesirable
procedure. To add proper perspective, it should
be observed that flamingos differ no more from
the Recurvirostridae than, for example, the An-
hingidae differ from the Sulidae, yet these last
two families are almost always included in the
same suborder of Pelecaniformes.
Therefore, we place the Phoenicopteridae in
the order Charadriiformes, suborder Charadrii,
immediately following the Recurvirostridae.
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