Table Of ContentTHE DISSECTION
OF VERTEBRATES
A Laboratory Manual
THIRD EDITION
G d I , Phd
erardo e ulIIs
Department of Ecology and Evolutionary Biology, University of Toronto;
Royal Ontario Museum; and George Brown College of Art and Technology
d P , MscBMC, CMI
Ino ulerà
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This book is for our spouses,
Virginia and Cinzia,
and children,
Daniel, Theodore, and Jacob,
whose love, support, encouragement, and infinite patience
were crucial for seeing this project to fruition,
and our parents,
Italo, Maria, Vittorio, and Pina,
for their love, support, and sacrifice
in providing us the opportunity to follow our dreams.
With deep respect, admiration, and gratitude, we dedicate this book to three teachers at the
University of Toronto, who early on in our academic paths instilled in us a passion for
anatomy, paleontology, and art as well as the intellectual discipline required to make these
passions our careers. Their contributions are evident throughout the following pages.
Charles S. “Rufus” Churcher
Stephen G. Gilbert
Thomas S. Parsons
To our readers:
Despite our best efforts, some errors are bound to have escaped our notice, and we would appreciate being
informed of these. We encourage you to contact us directly with your comments, suggestions, and possible ideas
for text and illustrations in future editions of this book.
We look forward to hearing from you.
Sincerely,
Dr. Gerry De Iuliis
[email protected]
Dino Pulerà
[email protected]
Preface
The resurgence of comparative vertebrate anatomy the actual hands-on experience. It is only through a care-
and the recognition of its broad value to many aspects of ful, patient, and repeated practical approach that we
biological inquiry, including the history of vertebrates, gain the expertise and practice required for understand-
have continued since the publication of the second edi- ing the spatial relationships that are essential to learning
tion of this manual—Budd and Olsson’s (2007:1) asser- how a vertebrate body is constructed, how its compo-
tion that there “has never been a better time to study nent structures are related to each other, and how form
morphology” rings truer than ever. Not only does ver- and function interact.
tebrate anatomy provide the only direct evidence for the There are those who would suggest that such a course
steps, sequence, and timing of the changes that occurred of study is unnecessary and that anatomy can be learned
during earlier parts of vertebrate evolution, but its value through texts or software. While such materials (this text
in helping elucidate the relationships among more recent among them) may prove invaluable as aids or tools for
members of the vertebrate clade is becoming increasingly learning, we ought not to substitute these adjuncts for
apparent among researchers, particularly those that the means through which we must come to know the
have often been dismissive of morphological data. This vertebrate body. To do so would be akin to preparing for
development, which might almost—somewhat face- an acting career by watching films, rather than through
tiously—be described as a radical change has, resulted in rehearsing and attending acting workshops. Few of us
several recent analyses that employ combined molecular would feel comfortable with mechanics trained solely
and morphological data sets in trying to determine ver- through the Internet, trust a surgeon who has learned
tebrate relationships. Unfortunately, however, the study the craft strictly through instructional videos, or fly with
of anatomy at the introductory and intermediate college a pilot who has only flown missions on a flight simula-
levels continues to suffer, and its stature and perceived tor. We would not be suspicious because we believe that
importance have yet to regain their luster. The reasons such instructional methods are not useful. Rather, we rec-
remain the same as those noted in earlier editions of this ognize that for fields whose subject matter includes com-
manual—regrettably, the trend at most major academic ponents arranged in complex spatial relationships, these
institutions has followed a path away from whole organ- media are meant to be used as tools that supplement
ismal biology, and positions related to vertebrate anat- and guide the trainee through a methodical, firsthand
omy seem to be fewer and farther between. Despite the experience with the subject matter itself. And science,
intense (and certainly justified) focus on genetics over of course, is an empirical endeavor. When practiced, sci-
the last several decades, it remains “clear that morphol- ence is based on observation and experience. If we are
ogy still stands at the heart of comparative biology. From to train students to become scientists, it is not sufficient
functional morphology to ultrastructure, morphological to merely present them with the products of science; we
topics link into ecology and physiology, developmental must engage students in actual scientific practice.
genetics and the fossil record; they connect them all” The debate on the value of dissection is particularly
(Budd and Olsson, 2007:1). lively for human medical anatomy (see, for example,
Increased resistance from some quarters to the use Sugand et al., 2010; Roseth and Saltarelli, 2014; Ross,
of animals in various scientific endeavors has also hin- 2015; Van Wyk and Rennie, 2015). Many researchers
dered introductory study in vertebrate anatomy. Further, are clearly in favor of dissection but also see the need
easily accessible computer software has been developed to incorporate the advanced imaging technologies cur-
that allows convenient visual journeys through verte- rently available. Indeed, a combination of the two tech-
brate bodies without the effort, expense, and “mess” of niques apparently leads to superior results (see Biasutto
actual dissection. et al., 2006). The same logic should apply for any verte-
The study of anatomy and morphology has much to brate, but similarly advanced technologies are unlikely
offer the student wishing to pursue a career in biological to be applied to a broad range of vertebrates in the fore-
or medical fields. Proper training in vertebrate anatomy seeable future.
must include a practical component that involves dissec- The central theme of most previous dissection manu-
tion, in addition to lectures. No other method, regardless als has been structural changes in vertebrates through
of how intricate in presentation and scope, can replace their evolution from fish to mammals, with the ultimate
xiii
xiv Preface
goal being to place mammalian anatomy in context. This in the vast majority of cases because illustration is the
is certainly a necessary prerequisite for one interested method that affords the most control in communicating
principally in mammalian systematics or medicine. the pertinent features of a particular dissection. Photos
However, not all students or instructors are interested are objective and indiscriminately record what the cam-
primarily in mammals. Two of the important lessons era sees, whereas illustrations (or rather the illustrator)
emphasized by phylogenetics are that all living verte- can be subjective, selective, and interpretative with the
brates have as long an independent evolutionary his- ability to omit unnecessary details and emphasize anat-
tory as mammals have, and that their anatomy has just omy important to the purpose of the dissection. Indeed,
as much to tell us about evolution, function, and mor- we have taken great care to ensure that the background
phology. Indeed, a common complaint among academic anatomy in the illustrations is accurate. This is important
faculty is that comparative vertebrate anatomy courses because it gives the users (instructor and student) a con-
have become courses on the anatomy of the cat. Be that text for the anatomical structures under study.
as it may, it is important to remember that negative per- Although students aspiring to careers in systemat-
ceptions can often be detrimental to the well-being of ics, vertebrate paleontology or functional morphology
a field of study and may sway departmental decisions are the primary intended audience of this manual, The
on whether the continuation of some courses is worth Dissection of Vertebrates is sufficiently flexible in scope
the effort and expense. It is up to those of us who teach and organization that it may be used in any course on
comparative anatomy to push forward and maintain its vertebrate anatomy. We present a wide-ranging and
vigor and centrality—in part by relating its wide appli- encompassing reference manual that will both help stu-
cability to related fields, such as systematics, evolution- dents learn the basic anatomy of vertebrates and func-
ary biology, paleontology, paleobiology, and functional tion as a guide once they are ready to venture into the
morphology—and as a prerequisite for higher level zool- primary literature.
ogy courses, such as mammalogy, herpetology, ornithol- The Dissection of Vertebrates presents dissection
ogy, ichthyology, developmental biology, and vertebrate instructions on more vertebrates than is normally the
paleontology. case, and this third edition also includes sections on
Our format and coverage is aimed at striking a bal- “prevertebrates”—a cephalochordate and a urochor-
ance between presenting an evolutionary sequence to date. The primary focus is on the shark, mudpuppy, and
“higher” vertebrates and the anatomy of each represen- cat, as is usual, but it also provides detailed information
tative vertebrate as inherently important. The sequence on vertebrates either not usually considered or treated
of vertebrates is similar to those presented by other very superficially by most other manuals that include
authors, but we must remember that living vertebrates multiple vertebrates. It is ironic that the two most spe-
are not and cannot be used as intermediates. For this ciose groups of vertebrates, birds and ray-finned fishes,
reason, we provide discussions of the important features are not adequately covered (if covered at all) in other dis-
of each group based on the derived features that diag- section manuals. We hope that by providing reasonably
nose a particular phylogenetic grouping. We thus do not detailed guides for these vertebrates, instructors will
treat vertebrates by traditional grouping methods; we feel more inclined to include these readily available and
would rather, from the beginning, present the student inexpensive vertebrates in their courses.
with information that reflects our formal thinking and This manual is organized by vertebrate. The anatomy
classification. of each is then presented systemically. This approach
The main goal of this text is to provide today’s visu- allows all the information on a particular vertebrate to be
ally oriented student population with a manual that studied at one time and in sequence. We believe, based
links succinct and pedagogically effective textual direc- on years of instruction, that this method provides a more
tion with relevant, accurate, and attractive visual ref- straightforward integration of the systems. The inclusion
erences to promote efficient learning of the complex, of many vertebrates and the organization by vertebrate
spatially abstract subject matter in the limited time makes The Dissection of Vertebrates more flexible for use in
available in a laboratory setting. Thus, a critical fea- a broad-based full or half-year course at the introductory
ture of The Dissection of Vertebrates is the inclusion of college level, and allows more convenient organization
numerous high-quality, didactic, color illustrations. of course content, depending on time and availability of
Each depicts the vertebrate approximately as it would specimens and the instructor’s preferences.
appear in a particular stage of dissection, rather than At the same time, we omit many topics that are often
presenting an idealized figure or photographs, as is the covered in most other manuals. Sections on vertebrates
case for most other manuals. This in itself facilitates the or structures that students are unlikely ever to dissect
use of these illustrations, both in learning and later dur- at the intended level of study are not included. Instead,
ing recall for studying purposes. Photographs are used we have focused the material on examples that are likely
sparingly. We have chosen illustration over photography to be encountered in an introductory lab course, leaving
Preface xv
those topics best presented in texts that accompany the this manual to their personal preferences in running their
lecture portion of a course. course. Structures that are not required can be identified
Much of the required background information is pre- and crossed out so students know they are not responsi-
sented in the Introduction and Chapter 1. This includes ble for them. This method effectively allows an instructor
sections on planes of dissection and orientational termi- to limit the detail of the dissection.
nology (see later), as well as an introduction to vertebrates We believe that the concise presentation of dissec-
and their relatives (Chapter 1). We suggest that these sec- tion instructions combined with minimal background
tions be included as part of the assigned readings for a information results in a straightforward text that will
particular laboratory for each vertebrate. This method facilitate and focus the student’s learning of anatomy in
will expose students repeatedly to the broad evolution- laboratory. In contrast to most other manuals, much of
ary development of each system. Terms that are required the background material presented in lecture is omitted
learning are placed in boldface print throughout the here, so The Dissection of Vertebrates is less cumbersome to
manual. Boldfaced terms are listed in a Key Terms section use even though it covers more vertebrates than do other
(which also provides common synonyms in parentheses) manuals. All the information is relevant for laboratory
following each major component. Students will know at purposes. This should facilitate matters for the instructor
a glance the structures for which they are responsible. We as well. Among other things, it will allow a clear answer
suggest that students use this section as a key to learn- to the often-asked question, “What am I responsible for
ing the structures by writing a short description for each. reading?” The response can be, without too much exag-
The Key Terms sections also allow instructors to adapt geration, “All of it.”
Acknowledgments
Many colleagues, students, friends, and members of the collections of the Royal Ontario Museum; Dr. Hans-
our families have contributed to the publication of the Rainer Duncker (Institut für Anatomie und Zellbiologie
first, second, and now third editions of this book, from der Justus-Liebig-Universität Giessen) for providing
carrying out simple tasks, to proofreading, to providing specimens of the avian air sac system and reviewing our
emotional encouragement and support. We are grateful illustrations (Figure 9.13); Dr. Walter Joyce (Universität
to them all, although we can directly acknowledge only Tübingen) for help with turtle skulls; Dr. Steven Huskey
a few of them here: Drs. Matthew F. Bonnan (Western (Western Kentucky University) for providing skeletal
Illinois University), Thomas Carr (Carthage College), specimens; Dr. Mathew J. Wedel (University of California
Randy Lauff (St. Francis Xavier University), Hans- Berkeley) for photographs of the pigeon air sac system
Dieter Sues (Smithsonian Institution), Jeff Thomason and reprint of a rare paper; Dr. Philip J. Motta (University
(University of Guelph), and Sergio F. Vizcaíno (Museo of South Florida) and students for their suggestions for
de La Plata) for their thorough, methodical, and thought- the second and third editions, and to Dr. Motta for kindly
ful reviews of earlier versions of this book and provid- allowing us to use the photo of the tunicate larva (Figure
ing valuable input on text and illustrations. We are also 1.28a); Dr. Barry Bruce (CSIRO Division of Marine
grateful to several anonymous reviewers for their help- Research, Tasmania), Mark McGrouther and Elizabeth
ful comments, suggestions, and corrections. Cameron (Australian Museum), and Andrew and Silvy
We are indebted to our intellectual forbears for impart- Fox (Rodney Fox Shark Museum, Australia) for pro-
ing not only their knowledge but for impressing upon viding shark dissection photos; a special thank you to
us the need for rigor and discipline, and to our many Dr. Steven E. Campana (University of Iceland) for also
colleagues for the resources they have produced—it is providing labeled shark dissection photos, and very
clear that we have leaned heavily on their efforts in pro- kindly allowing us to reprint the SEM photo of the spiny
ducing this manual. Many of their works are indicated dogfish skin (Figure 3.12f). We are grateful to Henry Hong
explicitly in the following pages, but several others, still and Audrey Chong of the Imaging Facility (Department
relevant and useful, are noted here. Prominent among of Cell and Systems Biology, University of Toronto) for
them is the work of the late Thomas S. Parsons and the late the use of several microscopes and help with micros-
Stephen G. Gilbert (e.g., Gans and Parsons, 1964; Romer copy. We also appreciate the assistance of Tim McGill
and Parsons, 1986; and Gilbert 1973a,b, 1974, 1989, 1991, (Leica Microsystems Canada) in the latter regard. We are
and 2000); both have had a strong influence on our lives also thankful to the many colleagues who took the time
and careers. In addition, we acknowledge the work of to write and point out errors in previous editions of this
Chiasson (1962, 1966, 1984), Chiasson and Radke (1993), manual, in particular Avery D. Franzen (University of
Cooper and Schiller (1975), Ecker (1971), Frank (1934), South Dakota), Dr. Rebecca Hartley (Seattle University),
George and Berger (1966), King and McLelland (1985), Dr. Randy Lauff (St. Francis Xavier University), Dr. Mark
Marinelli and Stregner (1954), Oldham and Smith S. Mills (Missouri Western State University), and
(1975), Romer (1997), Stuart (1947), Wake (1979), White Dr. Philip J. Motta (University of South Florida).
and Folkens (2005), Wyneken (2001), Wischnitzer and Sincere thanks to Drs. Rosana Moreira da Rocha
Wischnitzer (2006), and Zug et al. (2001). (Universidade Federal do Paraná) and Michael W.
We appreciate the efforts of Corey Goldman Konrad (Science is Art) for assistance with aspects of
(University of Toronto) and Dr. Cory Ross (George tunicate anatomy, and the former for also allowing
Brown College of Applied Arts and Technology) for aca- us to cite the Smithsonian Tropical Research Institute
demic and institutional support; Stephen Mader (Artery instructional video in Chapter 1; and Dr. Denis G. Baskin
Studios Inc.) for his encouragement and support; Peter (University of Washington School of Medicine) for assis-
von Bitter, Kathy David, Brian Iwama, and Peter Reali tance on aspects of cephalochordate anatomy.
for help with photography; Theodore and Jacob De Iuliis We appreciate the efforts of the following Elsevier staff
for their help in preparing specimens and photography; who have participated in this and previous editions of the
Daniel Pulerà for thoughtful suggestions on improving book: André Wolff, Mica Haley (Publishing Director - Life
some figures; Celestino De Iuliis for reading earlier drafts Sciences), Sandra Harron, Kiruthika Govindaraju, Lisa
of the manuscript; Dr. Marco Zimmer-De Iuliis for prep- Tickner, our former Elsevier partners Katie Fawkes, Janice
aration of specimens; Dr. Kevin Seymour for access to Audet, Sarah Binns, Mary Preap, and Andrea Cowan for
xvii
xviii Acknowledgments
patience, skill, guidance, and commitment to this project. own book, and for his encouragement, support, advice,
We are indebted to David Cella (former Publishing Director and continued inspiration. Lastly, we thank Virginia and
of Elsevier) for initial consideration of our proposal and Cinzia for being there beside us every step of the way in
recognizing the potential for this book, and to Stephen G. seeing the third edition of this book through to the end—it
Gilbert for showing us how to get started on creating our has been yet another long and challenging journey.
Introduction
The study of vertebrate anatomy is an interesting and (such as homology, for example), but also terms to des-
valid field of study for gaining insight into the struc- ignate unambiguously the orientation and direction of
ture and function of vertebrates. But why should this be structures of the vertebrate body. These terms may at
important? Of the numerous reasons, we shall mention first seem superfluous, but that is because most people
just a few: have never dealt with anatomy in a comprehensive and
detailed manner. It is perfectly adequate in everyday life
• It provides us with knowledge of the structures of
to say that the stomach is lower than the heart or the
different organisms and the great variety of form
appendix is in the lower right part of the belly. But this is
among vertebrates.
not anatomy. You will quickly come to realize the impor-
• It allows us to examine how the form of these
tance of the terms presented in this section, and you are
structures is related to their function and thus how
urged to learn, become familiar with, and use them.
morphology is suited to a particular mode of life.
There are two main sets of terms. One is used in
• The characteristics or features of vertebrates
medicine and by some anthropologists, the other by
preserve information on their ancestry; the features
comparative anatomists, paleontologists, and veteri-
are modified and passed on through the course
narians. To compound the problem, various synonyms
of generations, and we may use such knowledge
exist for some terms in each set. These circumstances
to discover the genealogical relationships among
may be cause for confusion, but we may simplify mat-
vertebrates.
ters by adhering to one set of terms. As we are studying
• Comparative anatomical studies help us understand
comparative anatomy, we will use the system commonly
how the major transitions in vertebrate design might
used for nonhuman vertebrates.
have occurred. Soft tissues do not fossilize, meaning
Unlike humans, the vast majority of vertebrates go
that (with rare exceptions) only transformations of
through life with the long axis of the body oriented hori-
the hard parts of the vertebrate body are preserved
zontally, parallel to the substrate. It is with reference to
in the fossil record. For other parts of the body, we
this position that the main directional terms are defined;
must rely on a sequence of living forms. There are
of course, these positions apply to the body, even though
problems with this approach, but if we begin with
it may not be in the position shown in Figure 1 (see later).
a robust phylogenetic hypothesis and keep in mind
Most of these terms are coupled; that is, there are two
that the living members of some groups are highly
terms that describe opposite directions along a single
derived, we may be confident in this method as a
axis. Refer to Figure 1 while reading the following expla-
reasonable approach for deducing the major steps in
nations. Anterior and posterior refer to the horizontal
the evolution of different vertebrate groups.
longitudinal axis and respectively designate the direc-
We will consider all these aspects in the following tions toward the head and tail. Synonyms for these terms
course on comparative vertebrate anatomy. Before begin- that you may encounter are cranial or rostral for anterior,
ning this study, however, we review several important and caudal for posterior. The vertical direction toward
terms that unambiguously describe position and direc- the belly or the ground is ventral; toward the back or
tion. These indispensable terms greatly facilitate navi- up is dorsal. Medial refers to the horizontal direc-
gating through the complex three-dimensional structure tion toward the sagittal midline (see later) of the body,
of vertebrate bodies. whereas lateral refers to the direction away from the
midline. These are the main terms, but another set also
is useful. Proximal and distal are terms often used with
DIRECTIONAL TERMINOLOGY a particular reference. At times this reference may be the
AND PLANES OF SECTION trunk of the body; at other times a particular structure,
such as the heart, may be the reference point. Proximal
As with all advanced fields of research, anatomical designates a position closer to the trunk or structure of
study requires the use of specialized terminology. Such reference; and distal farther from the trunk or structure
terminology includes not only special words for the ana- of reference. Thus, for example, the fingers (phalanges)
tomical structures themselves and concepts or processes are distal to the upper arm (brachium); and the proximal
xix
