Table Of ContentBiology and
Comparative Physiology of
B I R DS
Edited by
A. J. MARSHALL
Monash University
Victoria, Australia
VOLUME I
1960
ACADEMIC PRESS
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U.K. Edition pubUshed by
ACADEMIC PRESS INC. (LONDON) LIMITED
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Copyright © 1960 by Academic Press Inc.
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OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM THE PUBLISHERS
Library of Congress Catalog Card Number: 60-9073
Printed in Great Britain by W. S. Cowell Ltd, Ipswich, Suffolk
Contributors to Volume I
A. D'A. BELLAIRS, Department of Anatomy, St. Mary's Hospital Medical
School, University of London, England
RUTH BELLAIRS, Department of Zoology and Comparative Anatomy, St.
Bartholomew's Medical College, University of London, England
ANDREW J. BERGER, Department of Anatomy, The University of
Michigan, Ann Arbor, Michigan
DONALD S. FARNER, Department of Zoophysiology, Washington State
College, Pullman, Washington
C. R. JENKIN, Department of Anatomy, St. Mary's Hospital Medical
School, University of London, England
MARY E. RAWLES, Department of Embryology, Carnegie Institution of
Washington, Baltimore, Maryland
G. W. SALT, Department of Zoology, University of California, Davis,
California
D. L. SERVENTY, CSJ.B.O., Perth, Western Australia
J. R. SIMONS, Department of Zoology, University of Sydney, Australia
IVAN SPERBER, Boyal College of Agriculture, Uppsala, Sweden
ROBERT W. STORER, Museum of Zoology, The University of Michigan,
Ann Arbor, Michigan
W. E. SwiNTON, British Museum (Natural History), London, England
ERIK ZEUTHEN, Zoophysiological Laboratory, University of Copenhagen,
Denmark
V
Preface
It has become fashionable, and perhaps often necessary, for authors
and editors to apologise for new additions to the numerous—one could
perhaps better say multitudinous—^volumes that are already published
on the broader aspects of biology.
I do not propose to join the fashion. The genesis of the present book
lay in personal necessity. I had become extremely bored with the
frequent need to go back into the Victorian or Edwardian literature, or
to translate from another language, whenever I wanted a relatively
simple piece of information about a muscle, bone, the blood, gut or
sense organs of birds. Further, there was in no single volume even
moderately comprehensive accounts of the many—and often exciting—
ornithological discoveries made during the past thirty years.
For a while I thought of myself trying to write the sort of book that I
needed, but I soon decided that it would mean deserting my laboratory
for the library for at least five years. So, instead, I began to write to
friends and others whom I thought might like to contribute chapters to
such a volume. It was originally to have been called simply The Biology
of Birds but there are already pubHshed several books by that name and
so it became necessary to change it to the best alternative that we
could devise.
At first the book was meant to be issued in a single volume but it soon
became apparent that two would be a more convenient proposition.
It is designed not only for professional and amateur ornithologists, but
also for general biologists who will find in it at least some of the infor-
mation that they may need from time to time. A great deal of vital
physiological data on domestic birds is already obtainable in Sturkie's
Avian Physiology and the Romanoff's The Avian Egg and relatively
little of this is repeated by us.
Inevitably the present work is not completely integrated. There are
of necessity many omissions and again, some chapters overlap. A few
discrepancies occur that are hardly to be avoided when a number of
people, most of whom are actively engaged in adjacent fields are invited
to write precisely what they wish. Each author is responsible for the
facts and phraseology in his contribution, but neither he, nor most
emphatically the editor, is responsible for the spelling. Some of the
spelling employed (in particular the almost total avoidance of hyphens)
has resulted in brutalities that will seem to many people something like
the penultimate defeat of the English language.
My wife, Jane Marshall, has prepared many of the diagrams from
PREFACE
sketches or other material submitted by some of the authors, and during
the making of the book, Mr. C. M. Hutt and the staff of Academic
Press, London, have been enormously helpful to me.
To make the final due note of thanks is a melancholy task. While his
contribution was in galley proof, that friendly, humorous and talented
investigator, Gustaf Kramer, fell to his death while climbing in Italy.
His contribution is therefore not completely up to date. It has been seen
through the last stages by his former colleagues. Dr. Hildegarde
Maschlanka and Dr. H. G. Wallraff and to them I am grateful indeed.
June, 1960 A. J. MARSHALL
viii
Contents of Volume II
XIII The Central Nervous System BY ADOLF PORTMANN AND
WERNER STINGELIN
XIV Sensory Organs: Skin, Taste and Olfaction BY ADOLF PORTMANN
XV Sensory Organs: Vision and Audition BY R. J. PUMPHREY, F.R.S,
XVI The Endocrine Glands BY E. OTTO HOHN
XVII Sex and Secondary Sexual Characters BY EMIL WITSCHI
XVIII Reproduction BY A. J. MARSHALL
XIX Energy Metabolism, Thermoregulation and Body Temperature
BY JAMES R. KING AND DONALD S. EARNER
XX Fhght BY R. H. J. BROWN
XXI Breeding Seasons and Migration BY A. J. MARSHALL
XXII Long-Distance Orientation BY THE LATE G. KRAMER
XXIII Behavior BY R. A. HINDE
XXIV Bird Populations BY JOHN A. GIBB
xii
CHAPTER I
The Origin of Birds
W. E. SWINTON
I. Introduction 1
II. The Osteology of Archaeopteryx 1
III. The Relative Resemblances of Archaeopteryx to Reptiles and Birds 5
IV. Affinities with the Thecodontia 7
V^. Arboreal Adaptations 10
VI. The Development of Homoiothermy 11
VII. The Third Archaeopteryx 13
References 13
I. Introduction
The origin of birds is largely a matter of deduction. There is no fossil
evidence of the stages through which the remarkable change from reptile
to bird was achieved. That the birds owe their origin to reptiles can be
argued along two lines. First, the evidence of the oldest bird in the
geological record clearly indicates reptilian affinities. Second, if one
postulates the stages that would seem to be demanded by such an
evolutionary change, there are appropriate materials available in certain
reptile groups. Naturally these pieces of evidence are all deduced from
whole or partial skeletons, and the physiological changes that were
concomitant can be deduced from somewhat similar, but not necessarily
the same, reptilian groups.
At the outset it must be stressed that anatomical and physiological
conditions did not necessarily proceed at the same evolutionary rates
among those reptiles that gave rise to the birds or to the mammals; and
that comparisons between the fossil evidence and modern reptiles are
based ultimately upon the hinge of the jaws; upon the articular of the
lower jaw being hinged upon the quadrate of the skull. This reptilian
feature, though by convention it serves to distinguish reptiles from
mammals, is of no value as a criterion in birds. Neither is the general
arrangement or compactness of the skull bones, for there is at least one
instance in which a specimen is indistinguishably dinosaurian or avian.
It is important to establish the osteological features of Archaeopteryx
to determine the validity of their evidence.
II. The Osteology of Archaeopteryx
Archaeopteryx lithographica is known by four specimens. The first
specimen found was the imprint of a tail feather, part and counterpart,
B 1
2 W. E. SWINTON
and the separate pieces were acquired by the Berlin and the Munich
natural history museums. Then in 1861 the first skeleton was discovered
and this was shortly afterwards purchased by the British Museum.
Finally, in 1877, a somewhat more complete skeleton was discovered,
the so-called Archaeornis or Archaeopteryx siemensi, now also in the
Museum ftir Naturkunde, Berlin (see p. 13).
It is now clear that all these specimens are of the same genus and
species, Archaeopteryx lithographica von Meyer, and that all the speci-
mens are of the same geological age, namely Kimeridgian of the Upper
Jurassic.
Archaeopteryx was about the size of a crow, with a long and flexible
neck, a short and compact body, and a long reptilian tail decked with a
pair of feathers to each caudal vertebra.
There is little doubt that the skeleton would have passed as that of a
reptile but for the clear imprint of feathers. These have lately been
reassessed so that we can be clear as to the flying mechanism and abilities
of this strangely intermediate animal.
The London specimen shows the primary and secondary quills and
the coverts of the wings and the quills of the tail. All these are shown by
the imprint of their undersides. There are six primaries and ten secon-
daries. The tail quills extend from the sixth to the twentieth caudals,
making in all a feathered tail 300 mm. long and with a breadth at the
last vertebra of 80 mm. It is said that the tail quills are continuous with
a series of body feathers on the Berlin specimen but there is no evidence
for this on the London specimen. Nor is there any evidence of contour
feathers on either specimen, though reports of their existence have
been made by several writers.
In brief, the various characters oi Archaeopteryx are not in themselves
very remarkable. The skull, so far as it can be observed, has its sutures
closed for the most part, and the brain case is expanded, but the jaws
contain teeth implanted in sockets. The teeth of the London specimen
are elliptical in cross section and are based on a short pedestal, while
those of the Berlin specimen are round in section and without any
visibly expanded base. These differences are certainly due to the
mechanical pressure that the London specimen suffered after death,
and which resulted in the pushing up of the disrupted and flattened
teeth. It is clear that on the characters of skull and teeth, there are no
grounds for generic or specific differentiation between the London and
Berlin examples.
The closeness of the bone structure of the skull is matched by the
reptilian characters and positions of the cranial openings. There is a
well-marked premaxillary foramen and a large preorbital opening.
I. THE ORIGIN OF BIRDS 3
These are exactly like those of the archosaurs, particularly the dinosaurs.
There is a small mandibular foramen. The orbit is large with a well-
preserved ring of possibly fourteen sclerotic plates. The whole skull
must have been about 2 inches long.
This skull must have been borne at about right angles to the neck.
The number of cervical vertebrae cannot be defined. The column in the
London specimen is incomplete and only twenty-two precaudal verte-
brae have been identified. The column in the Berlin example is more
complete and would seem to comprise eighteen presacrals and the six
sacrals, five of which are fused. This suggests that the London specimen
lacks only two centra.
The centra themselves are small and amphicoelous. The tail is typically
reptilian and in both skeletons comprises twenty centra. Thus the tail
was only slightly less in vertebral length than the body and neck of the
animal, a fact that will be discussed later.
The ribs are imperfectly known, but abdominal ribs were present, and
these gastralia suggest a short sternum.
The shoulder girdle is represented by coracoids and scapulae, the
latter being three times as long as the former. This relationship and the
wide angle between the two is further evidence of the weakness of the
pectoral muscles.
The sternum was for long regarded as missing, but it has recently been
identified by Sir Gavin de Beer (or reidentified if it were the structure
observed by Marsh). The reconstruction of the complete pectoral girdle,
without the furcula, is shown in Fig. I. There the feebleness of the
Clavicle
Coracoid
•Sternum
FIG. 1. Pectoral girdle of Archaeopteryx.
whole structure is manifest. Petronievics included a keeled sternum as
one of the characters that defined the Berlin specimen as his new genus
Archaeornis, but he later reconsidered the statement and admitted that
this particular osteological feature was a supposition on his part.
The forelimb is well displayed upon the slab of the London specimen
4 W. E. SWINTON
and is remarkable for its length, which is almost that of the hindlimb.
One of the most interesting features, to be observed only in the London
specimen, is the condition of the third metacarpal, which is fused with
the carpal ossification, and thus represents a third carpometacarpus but
not the carpometacarpus such as is found in modern birds. The Berlin
specimen lacks this feature, but this is almost certainly due to the lesser
degree of ossification of that specimen, which is clearly a younger
bird. Otherwise, the fingers of Archaeopteryx were clawed. Although
the evidence of the feathers and the plumage is indisputable, the
forelimb really ended in a hand rather than in a functional wing as we
would understand it today.
The pelvic girdle is also clearly shown, all the bones being separate
from one another. The ilium is comparatively long and is concave
laterally, the preacetabular portion having a notch in its base for the
head of the pubis. The latter is long and pendant and united with its
fellow for nearly the distal half. The postacetabular part of the ilium is
short and sharply pointed; it had sutural connection with the ischium,
and the latter bone, though short and distally bifurcate, would appear
to have been continued in length during life by cartilage, so that the
two ischia were probably united distally.
The hindlimb is typically reptilian, with a femur almost exactly
three-quarters of the length of the tibia. The metatarsals are on the
average about half the length of the tibia, and each phalange roughly
a quarter of the tibial length.
There is some uncertainty as to the tibiotarsal and the tarsometatarsal
relationships, particularly as analyzed on the Berlin specimen by
Petronievics. It may be, however, that the proximal tarsal bones are
fused with the distal ends of the tibia and fibula, and the distal bones,
which are not recognizable, are presumably fused with the correspond-
ing metatarsals. These metatarsals are separate and unfused, though
side by side in the plantar plane. Thus if, as seems likely, the distal
tarsals are separately fused with the corresponding metatarsals,
Archaeopteryx has four separate tarsometatarsals.
There is little in such an arrangement to suggest that this primitive
bird retained any cursorial powers like those of dinosaurs, and, on the
other hand, the reversal of the first digit, or hallux, to a position back-
ward, and hence opposable to the other three digits, is clear evidence of
the arboreal and perching habits of Archaeopteryx,
Looking at the skeletal features of the two examples, it is now possible
to say that the main and only differences between the London and
Berlin specimens are the shape of the teeth, the slight differences in the
crista lateralis of the humerus and the flattening or otherwise of the
