<oological Journal
of (hP Linnean Sociefll
(1990), 98: 63--72. With 4 figures
Villi and the phyly of Wetmore’s order
Piciforrnes (Aves)
TIM G. BROM
Institute of Taxonomic <oology, University of Amsterdam, Mauritskade 61, 1092 A D
Amsterdam, The ,Wherlands
Received November 1988, accepted for publication December 1988
The occurrence of villi (outgrowths, projections) on the bases of thc hasalmost downy barbulcs of
breast-feathers is documented with scanning electron microscopy. T h e presence of these structurrs is
thought to constitute a synapomorphic character for Passeriformcs, Trochilidac, Capitonidac.
Indicatoridae, Ramphastidae, and Picidae, which once more casts suspicion on thc monophyl? of
Wetmore’s order Piciformes.
KEY WORDS: --Piciform birds
-
monophyly
microstructure of feathers
-~
~
\
illi.
CONTENTS
Introduction .
. .
Material and methods .
R e s u l t s . .
.
.
Discussion
. . .
Acknowledgements
.
References
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
63
6.1
.
.
65
. . . . . . . . . .
69
.
.
.
.
.
.
.
.
.
. 70
.
.
.
.
.
.
.
.
.
.
71
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
INTRODUCTION
In Wetmore’s (1960) widely accepted classification of birds, the order
immediately preceding the Passeriformes is that of the Piciformes. Within the
latter, the following six families are recognized: Galbulidae Cjacamars),
Bucconidae (puffbirds), Capitonidae (barbets), Indicatoridae (honeyguides),
Ramphastidae (toucans) and Picidae (woodpeckers, piculets and wrynecks).
Many authors considered this group of families to represent a natural assemblage
(e.g. Stresemann, 1927-34; Peters, 1948; Cracraft, 1981; Wolters, 1982). The
monophyly of the Piciformes has been based on a complex structural
modification of the foot involving the combination of a zygodactyl toe
arrangement, the Gadow Type VI flexor tendon pattern, a derived condition of
the M. flexor hallucis longus, and a well-developed ‘Sehnenhalter’ on the outer
trochlea of the tarsometatarsus (Garrod, 1875; Gadow, 1894; Miller. 1919;
Steinbacher, 1935; Bock & Miller, 1959; Simpson & Cracraft, 1981;
1981). Despite these apparently strong
Swierczewski & Raikow,
synapomorphies, the phylogenetic position of the Galbulidae and Bucconidae,
0024-4082/90/010063
+ 10 $03 00j0
63
0 1990 The Linnean
Societ\ ol London
64
T. G . BROM
and thus the monophyly of the Piciformes, has been questioned on
morphological (Furbringer, 1888; Olson, 1983; Burton, 1984) and biochemical
grounds (Sibley & Ahlquist, 1972, 1986; Lanyon & Zink, 1987; Prum, 1988).
Sibley & Ahlquist (1986) suggested that the Galbulidae and the Bucconidae
should be placed in a separate order. In their electrophoretic analysis of proteincoding loci in piciform birds, Lanyon & Zink (1987) found the average distance
between the galbulid and bucconid genera and the chosen outgroup Momotus to
be considerably smaller than the average distance between the other piciform
genera and Momotus. Although the polarity of biochemical distance data is
difficult to establish, these findings cast suspicion on the monophyly of
Wetmore’s order Piciformes. I t is evident that the phyly of the Piciformes and
their phylogenetic relationships to other birds are still open to discussion. The
Passeriformes and Coraciiformes are thought to be most closely related to the
Piciformes (Wetmore, 1960; Feduccia, 1977, 1979; Fig. l ) , but synapomorphies
corroborating the monophyly of this assemblage have not been described.
Feather characters have played only a minor role in the discussions on
piciform relationships. Nitzsch (1840), Shufeldt (1888) and Burt (1929)
summarized differences and similarities in pterylosis among several species of
woodpeckers, but these studies were confined to the family Picidae and did not
yield clear-cut characters which can be interpreted as either apomorphic or
plesiomorphic. Lowe ( 1939, 1946) compared feather tracts in Picidae,
Upupidae, Indicatoridae, Capitonidae, passeriforms, trochiliforms and
apodiforms, but failed to define clear-cut characters from which phylogenetic
relationships could be inferred. Haffer (1968) compared the moult of Aightfeathers in representatives of all six families and recognized two main lineages
among the piciform birds, one formed by the Galbulidae and Bucconidae, the
second by the four remaining families.
Several authors (Chandler, 1916; Lowe, 1939, 1946; Day, 1966; Reaney,
Richner & Cunningham, 1978; Brom, 1986) have studied the downy barbules at
the base of contour feathers of coraciiform, piciform, and passeriform birds. For
many species in these groups, minute outgrowths have been described from the
bases of the downy barbules. These outgrowths (not quite appropriately called
villi by Chandler, 1916) are highly variable in shape and are most abundant in
the proximal half or two-thirds of the barb. As a diagnostic character, villi play
an important role in the identification of bird remains (Brom, 1984, 1988). The
function of these projections remains unknown, although Reaney et al. (1978)
assumed that they serve to associate adjacent barbules.
The purpose of the present study is to document the distribution of villi among
Wetmore’s orders Passeriformes, Piciformes, Coraciiformes, Trogoniformes,
Coliiformes, Apodiformes, Caprimulgiformes, Cuculiformes and Psittaciformes,
and to assess its value for the determination of the phylogenetic relationships
between (some 00 these groups of birds.
MATERIAL AND METHODS
Downy barbules from breast-feathers of bird skins present in the Zoological
Museum Amsterdam have been examined with scanning electron microscopy
(SEM). As far as the material allowed, only feathers from adult birds were
selected. The barbules were mounted on aluminium stubs using double-sided
VILLI AND THE PHYLY O F PICIFORMES
65
tape, coated with gold/palladium for two to three minutes to provide a
conducting surface, and examined with an IS1 ds 130 scanning electron
microscope (accelerating voltage 10 kV, working distance 20 mm). The
following piciforms have been examined.
Galbulidae: yellow-billed jacamar Galbula albirostris Latham, 1 790, greentailed jacamar G. galbula (L., 1766), great jacamar Jacamerops a r e a (P.L.S.
Muller, 1776). Bucconidae: spotted puffbird Bucco tamatia Gmelin, 1788,
swallow-wing Chelidoptera tenebrosa (Pallas, 1782), crescent-chested puffbird
Malacoptila striata (Spix, 1822), black nunbird Monasa atra (Boddaert, 1 783),
white-eared puffbird Nystalus chacuru (Vieillot, 1816). Capitonidae: black-spotted
barbet Capito niger (P.L.S. Muller, 1776), red-headed barbet Eubucco bourcierii
(Lafresnaye, 1845), lemon-throated barbet E. richardsoni (G.R. Gray, 1846),
gold-whiskered barbet Megalaima chrysopogon (Temminck, 1824), brown-throated
barbet M . corvina (Temminck, 1831), great barbet &f.virens (Boddaert, 1783),
fire-tufted barbet Psilopogon pyrolophus S. Muller, 1835, toucan-barbet Semnornis
ramphastinus (Jardine, 1855), d’Arnaud’s barbet Trachyphorus darnauiii (Prkvost
and Des Murs, 1847), yellow-breasted barbet T. margaritatus (Cretzschmar,
1826). Indicatoridae: greater honeyguide Indicator indicator (Sparrman, 1777).
Ramphastidae: emerald toucanet Aulacorhynchus prasinus (Gould, 1834), Guiana
toucanet Selenidera culik (Wagler, l827), green araCari Pteroglossus viridis (L.,
1766), white-throated toucan Ramphastos tucanus L., 1758, toco-toucan R. toco
P.L.S. Muller, 1776, black-mandibled toucan T. ambiguus Swainson, 1823, keelbilled toucan R. sulfuratus Lesson, 1830, red-breasted toucan R. dicolorus L., 1766,
channel-billed toucan R. uitellinus Lichtenstein, 1823. Picidae: common flicker
Colaptes auratus (L., 1758), magellanic woodpecker Ipocrantor magellanicus (King,
1818), golden-fronted woodpecker Melanerpes aurifons (Wagler, 1829),
arrowhead-piculet Picumnus minutissimus ( Pallas, 1908), yellow-bellied sapsucker
Sphyrapicus varius (L., 1766), wryneck Jynx torquilla L., 1758, grey-headed
woodpecker Picus canus Gmelin, 1788, green woodpecker P. viridis L., 1758, black
woodpecker Dryocopus martius (L., 1758), great spotted woodpecker Dendrocopos
major (L., 1758), middle spotted woodpecker D.medius ( L . , 1758), lesser spotted
woodpecker D.minor (L., 1758), three-toed woodpecker Picoides tridactylus ( L . ,
1758).
The following outgroups were selected (number of species between brackets):
Coliidae ( 1) , Trogonidae (3), Musophagidae ( 1), Psittacidae (30),
Brachypteraciidae ( l ) , Coraciidae (2), Upupidae ( l ) , Phoeniculidae ( l ) ,
Momotidae (2), Bucerotidae (3), Bucorvidae (2), Alcedinidae (2), Meropidae
( 1 ), Trochilidae (8),Apodidae (2), Caprimulgidae (2), and Passeriformes ( 105,
including some suboscines such as chestnut-crowned antpitta Grallaria rujcapilla
Lafresnaye, 1842, black-crested antshrike Sakesphorus canadensis L., 1766, great
antshrike Taraba major (Vieillot, 1816) and fasciated antshrike Cjrnbilaimus
lineatus (Leach, 18 14)) .
RESULTS
The occurrence, distribution, and shape of villi at the bases of the basalmost
downy barbules of breast-feathers is presented in Table 1. In those birds where
these structures have been encountered, they are confined to the proximal
plumulaceous barbules of the main feather. In afterfeathers (or aftertufts) they
T. G . BROM
66
Y
(d
/
/
/
/
/
Figure 1. Wetmore's classification of Passeriformes, Piciformes, Coraciiformes, and Apodiformes,
represented as a phylogenetic tree.
are encountered only occasionally and in much lower numbers than in barbs of
the main feather. Villi are not randomly distributed over the surface of the bases,
but are confined to cell borders and consist of apical outgrowths of the cells
which form these bases (exactly as first described by Chandler, 1916, and
contrary to the description of Reaney et al., 1978; Figs 2D, E, F).
Villi in piciforms are highly characteristic being curved or scimitar-shaped
and their axis usually points backwards into the direction of the barb
(Fig. 2B, C, D). This type is found in Picidae, Indicatoridae and Capitonidae
(Chandler, 1916; Day, 1966; Reaney et al., 1978; Brom 1986; present study). The
most strongly developed villi are found in the Ramphastidae (Fig. 2D). In
ramphastids the villi are much longer than in any other bird, usually 20-25 pm
TABLE
1. Occurrence, distribution, a n d shape of villi in piciforms a n d related outgroups
Distribution
Presence
Galbulidae
Bucconidae
Capitonidae
Indicatoridae
Ramphastidae
Picidae
Passeriformes
Trochilidae
other outgroups
Base
Shape
Proximal part
Sharply
of pennulum Knobbed pointed
Direction towards:
Bifurcated
Base
Pennulum
VILLI AND THE PHYLY OF PICIFORMES
67
Figure 2. Scanning electron micrographs of bases of downy barbules of breast-feathers of Piciformes.
A, Green woodpecker Picus uiridis: pointed villi (“knobbed” appearance of left villus due to
attachment of keratin powder). B, Greater honey-guide Indicator indicator: pointed villi. C , Great
barbet Megalairnu uirens: recurved villus. D, Toco-toucan Ramphastos toco: strongly recurved villus. E,
Green-tailed jacamar Galbula galbula: smooth bases. F, Spotted puffbird Bucco tamatia: smooth bases.
Scale bars: A = S . I pm; B = 1 6 . 0 p m ; C = 2 . 2 p m ; D = 4 . 2 p m ; E = l l . O p m ; F = 2 2 . 0 p m .
long, but sometimes reaching a length of 35pm. I n feather preparations of
Galbulidae and Bucconidae no traces of villi have been observed (Chandler,
1916; this study), all bases being smooth (Fig. 2E, F ) .
Villi are present on the bases of downy barbules in all passeriform birds
investigated. Several hundreds of specimens have been examined (Chandler,
1916; Day, 1966; Reaney et al., 1978; Robertson, Harkin & Govan, 1984; Brom,
1986; this study), representing nearly all families of perching birds, and this
character has never been found missing. The shape of these villi is usually blunt,
knobbed or fingerlike, sharply pointed structures also occur. The villi always
point in the direction of the pennulum rather than to the barb (Fig. 3D). The
frequency, the position of the barbules with villi on the barb and the shape of the
68
T. G. BROM
Figure 3. Scanning electron micrographs of bases of downy barbules of breast-feathers of
Cuculiformes, Apodiformes, Passeriformes, and Trochilidae. A, African emerald-cuckoo C h r y s o c o c y
cupreus (Shaw, 1792): smooth bases. B, Whiskered tree-swift Hemiprocne mystucea (Lesson, 1827):
smooth bases. C, Blue-crowned motmot Momottcr momota (L., 1766): smooth bases. D, White wagtail
Motacillu alba (L., 1758): knobbed, bifurcated, and sharply pointed villi. E, Sword-billed
hummingbird Ensfera ensifera (Boissonneau, 1839): pointed villi, clearly visible as outgrowths of cell
borders. F, Gorgeted sunangel Heliangelus strophianus (Gould, 1846): knobbed and pointed villi at cell
borders. Scale bars: A = l l . O p m ; B=16.2pm; C=12.0pm; D =Il.Opm; E = 8 . 4 p m ; F = 6 . 3 p m .
villi all seem to vary among the different families of passeriforms, but an analysis
within this group is beyond the scope of this paper.
Quite unexpectedly, in view of the traditional association of Trochilidae and
Apodidae, villi have been encountered in all hummingbird species examined
(Chandler, 1916; R. C. Laybourne, personal communication; present study).
These villi are usually knobbed or fingerlike but sharply pointed and bifurcated
outgrowths also occur (Table l ) , and they point in the direction of the pennulum
(Fig. 3E, F). Trochilid villi are, however, not restricted to the base of the
barbule, b u t they can often be seen to continue on the proximal part of the
pennulum.
VILLI AND THE PHYLY OF PICIFORMES
69
In no other group examined have any traces of villi ever been found
(Fig. 3A-C).
DISCUSSION
For about a century, discussions on the phyly of the Order Piciformes have
been dominated by the study of osteological and myological characters, which
have been interpreted either as synapomorphies corroborating the monophyly of
the group (Simpson & Cracraft, 1981) or as convergent similarities (Olson,
1983). Other morphologically less complex, characters are therefore needed, the
interpretation of whose evolutionary polarity may prove to be less controversial
than traditional characters.
The structure of the downy barbules at the base of contour feathers is one of
the characters discussed by Lowe (1946). He seems to have interpreted the
similarities between Passeriformes, Picidae, Ramphastidae, Capitonidae and
Indicatoridae as what we now call synapomorphies; he did not study or even
mention the Galbulidae and Bucconidae. However, since he also stated that the
Hoopoe Upupa epops had ‘characteristic Passerine structures of barbules at base of
contour feathers-Passerine’, he evidently did not include villi in his summaries.
The characteristics probably meant concerned the nodal arrangement and
pigmentation of the barbules, features which at this level constitute
symplesiomorphies which become insignificant when evaluating the relationship
between Passeriformes and Piciformes.
From outgroup comparison, downy barbules with a smooth base evidently
represent the plesiomorphic condition and the possession of villi is apomorphic.
The presence of numerous downy barbules in a single feather establishes the
presence or absence of villi, the observations presented in this paper suggest that
a clear-cut synapomorphic character is present which supports the monophyly of
the group formed by Passeriformes, Trochilidae, Capitonidae, Indicatoridae,
Ramphastidae and Picidae (see Fig. 4). Admittedly, this hypothesis is based on
the study of a single character, which in fact may prove to exhibit some
homoplasy. However, with respect to the relationships between the six piciform
families of Wetmore (1960), these findings are congruent with the results of
Steinbacher ( 1 937), Burton (1984), Sibley & Ahlquist (1986), Avise & Aquadro
(1987) and Lanyon & Zink (1987), and therefore weaken the hypothesis that the
order Piciformes is monophyletic. Under the new definitions of poly- and
paraphyly proposed by Oosterbroek ( 1987), Wetmore’s order Piciformes should
be labelled as paraphyletic in case the passeriforms and trochiliforms prove to be
sister groups (Fig. 4), and as polyphyletic if they are not.
Villi may have been lost secondarily in Galbulidae and Bucconidae, although
this appears improbable. In this case the absence of villi on their downy barbules
should be interpreted as a loss and would therefore (for argument, see Pimentel
& Riggins, 1987) constitute an additional synapomorphy corroborating the
sister group relationship supposed by others (Simpson & Cracraft, 1981).
Most authors have considered the hummingbirds to be the closest relatives
(sister group) of the swifts (Nitzsch, 1840; Furbringer, 1888; Clark, 1906;
Stresemann, 1927-34; Wetmore, 1960; Kitto & Wilson, 1966; Cracraft, 1981;
Wolters, 1982). However, the question whether the observed similarities between
these groups are due to common ancestry or to convergence has remained
T. G. BROM
70
.-L
u
0
Q
6
a,
V
2
m
0
a
m
fa
0
\
/
Y
/
/
/
/
Figure 4. Phylogenetic relationship between Passeriformes, Trochilidae, and four piciform families,
as suggested by the presumed apomorphic presence of villi. For postulated relationships between
Picidae, Indicatoridae, Ramphastidae, and Capitonidae, see Simpson & Cracraft (1981) and Prum
( 1988).
unsolved, and also the affinities to other groups is obscure (review by Sibley &
Ahlquist, 1972). The presence of villi at the downy barbules of hummingbird
feathers was first noticed by Chandler (1916). He did not discuss the affinities
between Trochilidae and Apodidae, but assumed that the hummingbirds are
closely related to the Passeriformes. Nevertheless, in his ‘phylogenetic tree’
(Chandler, 1916: 391) he did not assign decisive weight to his observation ofvilli,
for he placed the hummingbirds with the Coraciiformes. Since villi are
polymorphic in shape, even within a single feather (Table l ) , it is not possible to
define the plesiomorphic and apomorphic condition of this character, and it
remains unclear whether the hummingbirds are best considered the sister group
of either the Passeriformes or the Piciformes, or both of them. Therefore, it is
suggested that future studies on the relationships of Passeriformes and Piciformes
should also pay attention to representatives of the Trochilidae.
ACKNOWLEDGEMENTS
Thanks are due to the Department of Electron Microscopy and Molecular
Cytology, University of Amsterdam, for the use of facilities; to Johan Leutscher
and Wijnand Takkenberg for technical assistance; and to Dr Jan Wattel
(Curator of the Bird Department, Zoological Museum, Amsterdam) for the
opportunity to study material under his care. Renk W. R. J. Dekker, Ronald
Sluys, and Jan Wattel provided valuable comments to earlier versions of the
VILLI AND T H E PHYLY OF P I C I F O R M E S
71
manuscript; Tineke G. Prins and J. Zaagman kindly assisted in preparing the
illustrations. The investigations were supported by the Foundation for
Fundamental Biological Research (BION), which is subsidized by the
Netherlands Organization for Scientific Research (NWO).
REFERENCES
AC'ISE, J. C . & A Q L - h D R O , C:. F.,1987. Sfalatr dehydrogenase isozymcs proiidr a ptiylogrnctic marker lor
the Piciformes (woodpeckers and allies). Auk, 104: 324-328.
BOCK, W. J . & M I L L E R , W. D., 1959. T h e scansorial foot of thr woodpeckers. wilh rommcnts on the
evolution of perching and climbing feet in birds. American Museum Nouitates, 1931: 1-45.
BROM, 'I. G., 1984. Microscopic identification of &:athers in order to improve birdstrikr statistics. I n M.J.
Harrison, S. A. Gauthreaux & L. 4. Abron-Robinson (Eds), Proceedingj Wildlije Hazard.{ to Aircraji Conference
and Training Mbrkshop, Charles/on, S.C.: 107-1 19. Springfield Virginia: National Tcchnical Information
Service.
BROM, T. G., 1986. Microscopic identification offcathers and feather fragments of I'alearctic birds. Bcldragm
tot de Dierkunde, 56: 181-204.
BROM, 7'. G., 1988. T h e analysis of feather remains: evaluation and prrspcctiws. 19th Meeting Bird Strike
Committee Europe. .\fadrid, Working Paper, 24: 1-14.
BURT, W. H., 1929. l'terylography of certain North American woodpeckers. [,-nii.rrii(y a/ (.'alzJornin Puhli(ntions
in <oology, 30: 427 442.
B U R T O N , P. J . K.. 1984. Anatomy and evolution of the feeding apparatus in the avian orders Corariilbrmes
and Piciformes. Bulletin of' the British Musrum (,V'atural History), <ooloLgy, 47: 331-443.
r their taxonomic signifirancc.
CHANDLER, A. C.. 1916. A study of the structure of feathers, with r e t ~ e n c to
University of' California Publication5 in ,S0010gy, 13: 2.13446.
CLARK, H . L.. 1906. T h r frather tracts of swifts and hummingbirds. A u k , 23: 68-91.
CRACRAFT, J., 1981. 'l'oward a phylogenrtic classification of the reccnt birds of the world (Class A \ r s . .4uk.
98: 681-714.
DAY, M. G., 1966. Identification of hair and feather remains in thr gut and facccs of stoats aiid wrascls.
Journal of<oology. London, 148: 201-217.
FEDUCCIA, 4 . , 1977. A model for the evolution of perching birds. Systematzc ~ o o l o g y ,26: 19 3 1
FEDUCCIA, A , , 1979. Comments on the phylogeny of perching birds. Proreedings of the BiolqiSicni S o ( v ! y o j
Washington, 92: 689-696.
FURBRINGER, M..1888. Untcrsuchungen zur Morphologie und Systcmatik dcr Vogcl, zuglcich v i i i Rcitrag
zur Anatomie der Stutz- uiid Brwrgungsorgane. Amsterdam: van Hoikcma. [Also apprarrd in Bijdrngm tot
de Dierkunde, 15, 1888.J
GADOW, H., 1894. \luscular system. I n A. Newton (Ed.), d Dictiona[y oJBirds: 602-620. London: Adam and
Charles Black.
G A R R O D , A. H.. 1875. O n thc disposition of the deep plantar tendons in differrnt birds. lJrouediq\ u / the
<oological SoczeQ of London, 1875: 339-348.
HAFFER, J,, 1968. c b e r die Flugel- und Schwanzmausrr columbianischer Piciformes. j'ournal,fur O?ni/ho/ogzt.
109: 157--171.
KIT'IO, G. B. & \\ILSC)N, A. C., 1966. Evolution of malate dehydrogenase in birds. Science, 173: 1408 1410.
LANYON, S. M. & ZINK, R . M.,1987. Genetic variation in piciform birds: monophyly and gciicric and
familial relationships. A4uk, 104: 7 2 4 7 3 2 .
LOWE, P. R . , 1939. O n the systematir position of the swifts (suborder Cypselii and humming hirds auhordrr
Trochili), with spccial reference to their relation to the order Passeriformes. Transactions of' the ;oological
SocieQ of London, 24: 307-348.
LOWE, P. R . , 1946. O n thc systrmatir position of the woodpeckers (I'ici). honcy-guidcs (Indicator . ~ ( J O ~ C J C S
and others. Ibis, 88: 103-127.
M I L L E R , W. deM'.. 1919. 'I'hc deep plantar tendons in the puff-birds, jacamars arid ltrcir a1lic.a. .luk, 36:
285-286.
NITZSCH, C. L.. 1840. System der Pterq.lographie. Halle a. S.: Edouard Anton.
O L S O N , S. L., 1983. Evidence for a polyphyletic origin of the Piciformes. A u k , 100: 126-133.
O O S T E R B R O E K , P.. 1987. More appropriate definitions of paraphyly and polyphyly. with a rommrnt on
the Farris 1974 model. Systematic .Soo/o,g, 36: 103%108.
PETERS, J. L., 1948. Check-list of Birds of the M/orld, V f . Cambridge: Harvard Lni\crsity Prrss.
L, R . 4 . & RIGGINS. R.. 1987. T h e nature nf cladistic data. CladisticJ, 3: 201-209.
P R U M , R. O., 1988. Phylogenetir interrelationships of the barbets (Avrs: Capitnnidae) and toucans h v e i :
Ramphastidae) based on morphology with comparisons to DNA-DNA hybridization. <oohJ~@'a/ ~7ournalUJ
the Linnean Society, 92: 313 343.
REANEY, B. A,, R I C H N L R , S. M. & CUNNINGHAM. LV. P., 1978. A prrliminar) scanniiig electron
72
T. G. BROM
microscope study of the minute morphological features of feathers and their taxonomic significance. Scanning
Electron Microscopy, 11: 47 1-478.
ROBERTSON, J., HARKIN, C., & GOVAN, J., 1984. The identification of bird feathers. Scheme for feather
examination. Journal of the Forensic Science Sociey, 24: 85-98.
SHUFELDT, R. W., 1888. Observations on the pterylosis of certain Picidae. Auk, 5: 212-218.
SIBLEY, C. G. & AHLQUIST, J. E., 1972. A comparative study of the egg white proteins of non-passerine
birds. Peabody Museum of Natural History Bulletin, N o . 39.
SIBLEY, C. G. & AHLQUIST, J. E., 1986. Reconstructing bird phylogeny by comparing DNA’s. SczentiJic
American, 254: 82-92.
SIMPSON, S. F. & CRACRAFT, J,, 1981. The phylogenetic relationships of the Piciformes (class Aves). Auk,
98: 481-494.
STEINBACHER, G., 1935. Funktionell-anatomische Untersuchungen an Vogelfussen mit Wendezehen und
Riickzehen. Journal f u r Omithologie, 83: 2 14-282.
STEINBACHER, J., 1937. Anatomische Untersuchungen iiber die systematische Stellung der Galbulidae und
Bucconidae. Archiu f u r Naturgeschichte (N.F.), 6: 41 7-5 15.
STRESEMANN, E., 1927-34. In W. Kiikenthal (Ed.), Handbuch der Zoolosie 7. Berlin & Leipzig: de Gruyter &
co.
SWIERCZEWSKI, E. V. & RAIKOW, R. J., 1981. Hind limb morphology, phylogeny, and classification of
the Piciformes. Auk, 98: 46-80.
WETMORE, A., 1960. A classification for the birds of the world. Smithsonian Miscellaneous Collections, 139, 11:
1-37.
WOLTERS, H. E., 1982. Die Vogelarten der Erde. Hamburg: Paul Parey.