Reptilian Lungs: Functional Anatomy and Evolution

90 Pages·1983·4.421 MB·English

by  Steven F. Perry Ph.D. (auth.)

Advances in Anatomy
Embryology and Cell Biology
Vol. 79
Editors
F. Beck, Leicester W. Rild, Galveston
J. van Limborgh, Amsterdam R. Ortmann, K61n
J.E. Pauly, Little Rock T.R. Schiebler, Wiirzburg
Steven F. Perry
Reptilian Lungs
Functional Anatomy and Evolution
With 32 Figures
Springer-Verlag
Berlin Heidelberg New York 1983
Steven F. Perry, Ph. D.
Fachbereich Biologie der Universitiit
Ammerlander Heerstr. 67-99
D-2900 Oldenburg
Dedicated to my best friend and companion, D. E.
Revised and augmented version of the "Habilitationsschrift
zur Erlangung der venia legendi im Fachgebiet Zoologie, Fach
bereich Biologie, der Universitat Oldenburg"
ISBN -13: 978-3-540-12194-7 e-ISBN -13 :978-3-642-68964-2
DOl: 10.1007/978-3-642-68964-2
Library of Congress Cataloging in Publication Data
Perry, Steven F., 1944 - Reptilian lungs.
(Advances in anatomy, embroyology, and cell biology; v. 79)
Thesis (habilitation) - Universitat Oldenburg.
Bibliography: p. Includes index. 1. Reptiles - Anatomy. 2. Reptiles -
Evolution. 3. Lungs. I. Title. II. Series. [DNLM: L Evolution. 2. Lung -
Anatomy and histology. 3. Lung - Physiology. 4. Reptiles - Anatomy
and histology. 5. Reptiles - Physiology. WI AD433K v. 79/QL 665 P465r)
QL801.E67 vol. 79 [QL665) 574.4s [597.9'0442)83-503
ISBN-13:978-3-540-12194-7 (U.S.)
This work is subject to copyright. All rights are reserved, whether the
whole or part of the material is concerned, specifically those of transla
tion, reprinting, re-use of illustrations, broadcasting, reproduction by
photocopying machine or similar means, and storage in data banks.
Under § 54 of the German Copyright Law where copies are made for
other than private use, a fee is payable to "Verwertungsgesellschaft
Wort", Munich.
© Springer-Verlag Berlin Heidelberg 1983
The use of general descriptive names, trade names, trade marks, etc. in
this publication, even if the former are not especially identified, is not to
be taken as a sign that such names, as understood by the Trade Marks and
Merchandise Marks Act, may accordingly be used freely by anyone.
Product Liability: The publisher can give no guarantee for information
about drug dosage and application thereof contained in this book. In
every individual case the respective user must check its accuracy by
consulting other pharmaceutical literature.
Composition: Schreibsatz Service Weihrauch, Wiirzburg
2121/3321-543210
Contents
Acknowledgments ......................... VII
1 Introduction . . . . . . . . . . . . . . . . . . . . ...
1.1 Functional Anatomy and the Evolution of the
Respiratory System. . . . . . . . . . . . . . . . . . .
1.2 Descriptive Classification of Lung Types .... .
1.2.1 Parenchymal Types . . . . . . . . .......... . 2
1.2.2 Functional Suspension of the Lung Within the
Body Cavity and of the Partitions Within the
Lung ........................... . 3
1.2.3 Histological Structure ..... . . . . . . . . . . . . 3
2 Morphometry of Reptilian Lungs,
with Special Emphasis on the Comparison of
the Unicameral Lungs of the Teju, Tupinambis
nigropunctatus Spix, and the Multicameral
Lungs of the Savanna Monitor, Varanus exan
thematicus (Bosc) . . . . . . . . . . . . . . . . . . . . 8
2.1 Animals ......................... . 8
2.2 Symbols and Definitions .............. . 10
2.3 Morphometric Methods . . . . . . . . . . . . . . . . 11
2.3.1 Techniques ....................... . 12
2.3.1.1 Preparation of Tissue. . . . . . . . . . . . . . . . . . 12
2.3.1.2 Morphometry of Major Parameters for
Comparison of Lungs and Lung Regions ..... 13
2.3.1.3 Application of Primary (Measured) Parameters: 19
2.3.2 Discussion of Morphometric Methods ...... . 20
2.4 Morphometric Results . . . . . . .......... . 22
2.4.1 Relationship Between Lung Volume and
Structural Type . . . . . . . . . . . . . . . . . . . . . 22
2.4.2 Volumetric Relationship of Central Lumen
to Parenchyma . . . . . . . . . . . .......... . 22
2.4.3 Parenchyma 23
2.4.3.1 Distribution Within the Lung ........... . 23
2.4.3.2 Parenchymal Volume, Surface Area, Surface
to-Volume Ratio, and Equivalent Parenchymal
Thickness ........................ . 25
2.4.3.3 Growth Patterns. . . . . . . . . . . . . . . . . . . . . 26
2.4.3.4 Volume Relationships Within Parenchymal
Tissue. . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
2.4.3.5 Analysis of Parenchymal Surfaces ......... 29
2.4.3.6 Anatomical Diffusion Factor ............ 36
V
Degree of Exploitation of the Lung ....... . 37
2.5 Discussion: Morphometric Comparison of
Reptilian Lungs . . . . . . . . . . . . . . . . . . . . . 39
2.5.1 Lung Volume ...................... . 39
2.5.2 Parenchymal Volume ................ . 40
2.5.3 Surface-to-Volume Ratio in Parenchyma and
Respiratory Surface Area . . . . . . . . . . . . . . . 42
2.5.4 Harmonic Mean Thickness ofthe Air-Blood
Tissue Barrier. . . . . . . . . . . . . . . . . . . . . . . 42
2.5.5 Capillary Bulging ...... . . . . . . . . . . . . . . 42
2.5.6 Strategy in Sequence of Anatomical Adapta-
tions for Gas Exchange by Diffusion ...... . 43
2.5.7 Pulmonary Smooth Muscle ............. . 46
2.6 Summary ........................ . 47
3 The Pump Mechanism, Its Combination with
the Exchanger, and Breathing Strategy ..... . 48
3.1 Symbols and Definitions .............. . 48
3.2 The Pump ........................ . 49
3.3 Breathing Strategy and the Pump ......... . 53
3.4 Interaction of the Exchanger and Pump in
Breathing Strategy: the Ideal High-performance
Lung ........................... . 53
4 Speculations on the Evolution of the Amniote
Respiratory System .................. . 60
4.1 Breathing Mechanism in the First Reptiles . . . . 60
4.2 Lung Structure in the First Reptiles . . . . . . . . 60
4.3 Hollow Bones as Indicators of Lung Structure 62
4.4 Possible Respiratory Function of the Gastralia 62
4.5 Possible Role of the Ornithischian Pelvis in
Breathing ........................ . 64
4.6 Broadened Ribs and Alternative Breathing
Mechanisms ....................... . 64
4.7 Implications for the Evolution of Lung
Structure ........................ . 65
s Summary 66
References .............................. 68
Subject Index ............................ 73
VI
The author gratefully acknowledges the expert assistance of
Mrs. A Riese with the electron microscope and of Miss 1. Zaehle
in morphometric evaluation, as well as the help of Mrs. S. Wil
lig in production of illustrations. Mrs. C.P. Komer deserves
special mention of her patient and expert secretarial assistance.
The Subject Index was compiled under the competent help
and guidance of Dipl. Phys. H. Allers (Fachreferent ftiT Biologie,
BIS, Oldenburg) and with cooperation of the computer center.
The advice of Prof. H.-R. Duncker and his fmancial assistance
through the Deutsche Forschungsgemeinschaft (Du 50/3 and
Du 50/4) were invaluable to this work. The Deutsche Forschungs
gemeinschaft also supported the completion of this work by
a research grant to the author (Pe 267/1).
VII
«Tout etre organise forme un ensemble, un systeme unique et
clos, dont to utes les parties se correspondent mutuellement, et
concourent It ]a meme action defmitive par une reaction reci
pro que. Aucune de ces parties ne peut changer sans que les
autres changent aussi; et par consequent chacune d'elles, prise
separement, indique et donne toute les autres.»
Cuvier (1812)
1 Introduction
1.1 Functional Anatomy and the Evolution of the Respiratory System
No organ system can be completely understood if it is considered isolated from all
others. By the same token, the interrelationship in structure and function within and
among organ systems can be used in order to validate assumptions concerning one sys
tem based upon information from another (Cuvier 1812). Furthermore, most
anatomical differences between related organisms can be explained in terms of allo
metric modifications of structural entities already present in their common ancestor
(Thompson 1951). These two principles - the structural and functional integrity of
the organism and the dependence of any given structure upon the phylogenetic herit
age of the organism - are cornerstones of comparative anatomy. Traditionally, the
latter has been emphasized and employed to determine systematic relationships
(Hennig 1966). In the present work such previously determined relationships among
major groups will be tentatively assumed correct. Within this framework, the structure
function relationship will be examined in detail in the respiratory system of two
species of lizard in which the lung structure is fundamentally different. These correla
tions will then be extended to other organ systems, including the locomotor system, in
these and other species. Finally speculation regarding the possible structure of lungs
in certain extinct species will be risked.
1.2 Descriptive Qassification of Lung Types
Implicit in the study of the evolution oflung structure is the assumption that different
types of lungs can be identified and that one type can give rise to another in response
to different physiological demands. It is therefore necessary, before considering the
question of lung evolution, to descriptively characterize certain structural types
(Fig. 1). Duncker (1978b) proposed a type-classification system similar to that em
ployed by Milani (1894, 1897) almost 90 years ago. The lungs of all mammals are
basically similar in structure: bronchoalveolar. The respiratory system of all birds, on
the other hand, can be designated as a lung-air-sac system; the lung itself as para
bronchial.
The array of lung structures seen among reptiles (Fig. 1) is too complex to be de
scribed in a single word. The simplest lung type, present in the only surviving rhyncho-
1
JlI<tSSC
~~)
Unicameral
~COJ
Paucicameral
~~
Multicameral
Lung-air-sac system
Bronchoalveolar Parabronchiallung
Fig. 1. Simplified phylogenetic tree of major amniote groups, showing schematic structural types
of lungs of living representatives
cephalian, Sphenodon, and in most families of lizards, is the unicameral lung. This
type possesses a single, undivided central lumen and the respiratory surfaces are elabor
ations of the lung wall: primary partitions. A second type is the paucicameral lung,
in which the central lumen is divided by a small number of large septa. Such lungs are
found among chameleons (Klaver 1973), agamids, and iguanids. The concept of
"a small number of large septa" is a relative one, and thus the distinction between uni
cameral and paucicameral lungs admits of transitional forms, such as those described
in chameleons and brookesians (Klaver 1973, 1977, 1979). A third reptilian lung type
seen in crocodilians, varanids, and chelonians, is the multicameral lung. Here the
cartilage-reinforced, intrapulmonary bronchus or duct connects with a number of
separate chambers. The tracheal lung of many snakes (Brongersma 1957a, b; 1960)
is classified as unicameral in spite of the presence of an intrapulmonary trachea (extra
tracheal lung!) because discrete chambers are lacking.
1.2.1 Parenchymal Types
The parenchyma of mammalian lungs has long been characterized as alveolar. The
intertwining air capillaries and blood capillaries of the bird lung are referred to as the
blood-air-capillary net (Duncker 1972). In the reptilian lung, the simplest type is the
trabecular parenchyma, in which branching, muscular structures called trabeculae
(Perry 1972) lie directly on the lung wall, where they form a polygonal network. If
2
the trabeculae are raised above the inner lung surface, a system of large polygonal
cubicles (ediculae) results and the parenchyma is termed edicular (Duncker 1981).
Through secondary and tertiary branching of the trabeculae and a deepening of the
parenchyma, a honeycomb-like appearance is attained. Such a parenchyma is termed
faveolar, and the air spaces within it, faveoli (Duncker 1978b). Trabecular parenchyma
is typical of urodele lungs but may also be found in some thin-walled, membranous
regions of reptilian lungs. Edicular parenchyma is found in the lungs of anurans and
of Sphenodon, but is also seen in the multicamerallungs of crocodiles, monitors, and
some turtles. Faveolar parenchyma is typical of active reptiles which possess uni
cameral lungs, such as teiids, lacertids, skinks, and snakes.
This descriptive characterization of parenchymal types is too subjective to meet
all the needs of a morphometric study; therefore, a more objective, ifless economical,
system will be introduced here. First, the parenchyma will be classified, according to
its distribution within the lung, as homogeneous or heterogeneous. Secondly, in lieu
of parenchymal types, the mode of "partitioning" will be described as sparse or dense,
shallow or deep. Thus, a typical edicular parenchyma, such as that of a frog lung, can
be characterized as a homogenously distributed, sparsely partitioned, deep parenchyma.
The faveolar-trabecular parenchyma of a typical snake lung would be characterized
as a heterogeneously distributed, densely partitioned parenchyma which is deep
cranially and shallow caudally.
1.2.2 Functional Suspension of the Lung Within the Body Cavity and of the Partitions
Within the Lung
In an air-filled lung in which the glottis is closed, contraction of trabecular smooth
muscle Simultaneously pulls the partitions taut and increases the intrapulmonary air
pressure equally in all parts of the lung. This increased air pressure allows the lungs to
maintain a characteristic shape and volume within the pleuroperitoneal cavity. If the
distribution of muscle bundles and of parenchyma over the pulmonary surface approx
imates uniformity, the lung will be intrinsically stable. Such lungs - whether unicameral
(e.g., teju, Lacerta), multicameral (e.g., snapping turtle, crocodile), or bronchoalveolar
(mammals) - may be only loosely attached to the pleuroperitoneal wall or freely sus
pended in pleural spaces (Duncker 1978a).
If the distribution of muscle bundles and of parenchyma is not uniform, the
regions having little such tissue would tend to become overinflated at the expe.nse
of densely partitioned regions. Thus, heterogeneously partitioned respiratory systems
of all structural types tend to be attached to the body wall and to the intracoelomic
septa surrounding them (Duncker 1978a; Perry and Duncker 1980). Included in this
category are snakes, monitors, and birds.
1.2.3 Histological Structure
The histological and fine structure of the lungs in all vertebrate classes has been
studied in some detail. The early studies, such as that of Ogawa (1920), dealt with the
complete histological structure of the lung, including the distribution of smooth
muscle and elastic tissue. Although a small number of studies in recent years have been
on this broad level (Perry 1972; Klemm et al. 1979), the majority of descriptive
3