LAB 7
Testudines
AMNIOTA: REPTILIA
(CHELONIA, LEPIDOSAURIA, AND ARCHOSAURIA)
Ignore material on this page
MATERIALS
- Lo\:\o(\
-t
1.
2.
3.
4.
Various whole-skeletons of chelonians, squamates, and archosaurs.
Various ethanol-preserved reptilians for examination.
Preserved snake and bird for dissection.
Read Chapter 12 (pages 342-367), Chapter 13 (pages 368-418), Chapter 15
(pages 425-467), and Chapter 17 (pages 487-515) in Pough et al. (1999).
"The amniotic egg . . . was a major innovation in vertebrate history, to be compared
with the appearance of (jaws], or the migration of backboned animals from the water on
to the land."
-")
~(::' "",{)(:;I 0':1.
0·' \\('.tc'
't),. 0
- Edwin Colbert and Michael Morales, 1991
t
(
SUMMARY CLASSIFICATION
~ Wc..)(.~-"d
Amniota is comprised of Reptilia and Mammalia. This lab provides a
general overview of reptilian diversity and highlights the major clades with
taxonomic representatives of each - only a glimpse of overall diversity is
possible. Lab 8 will review mammalian diversity. The following summary
classification lists only those taxa which have been chosen for review in this
lab. See cladograms presented in this lab and references for more complete
taxonomic coverage.
1-lJ,C-+ Ie..,
-~ HOt P
-\- l (i;;~
-
[:'Sox
t:os'l'ec
'r
Ie...
Amniota - amniotes
Mammalia - Lab 8
Reptilia - reptilians
177
Sauropsida
Testudines
These two -oidea
names contain
families we talked
about in lecture,
consult your notes
for family names.
178
Chelonia - chelonians
Pleurodira - sideneck turtles
Cryptodira - cryptodires
Chelydridae - snapping turtles
Chelonioidea - sea turtles
Testudinoidea - includes tortoises, box, and slider turtles
Trionychoidea - includes softshell, musk and mud turtles
Sauria - saurians
Lepidosauria - lepidosaurs
Sphenodon - tuatara (two extant species)
Squamata - squamates
Iguania - iguanians
Iguanidae - iguanas, includes chuckwallas and others
Phrynosomatidae - includes horned and spiny lizards
Polychridae - anoles (all New World)
Chamaeleonidae - includes true chameleons (all Old World)
Scleroglossa - scleroglossans
Gekkota - geckos and pygopods
Autarchoglossa
Scincomorpha - includes skinks, whiptails, and night lizards
Anguimorpha - alligator, beaded, and monitor lizards
Serpentes - snakes
Archosauria - archosaurs
Crocodylia - crocodiles, alligators, caimans, and gavials
Aves-birds
Struthioniformes - ratites, such as ostrich, rheas, and kiwi
Anseriformes - includes ducks, geese, and swans
Passeriformes - includes sparrows, warblers, and thrushes
Piciformes - woodpeckers
Strigiformes - owls
Psittaciformes - parrots
Charadriiformes - includes shorebirds, gulls, and terns
Columbiformes - pigeons and doves
Falconiformes - hawks, eagles, falcons, and vultures
Apodiformes - hummingbirds and swifts
Pelecaniformes - includes pelicans, cormorants, and boobies
Sphenisciformes - penguins
LABS FOR VERTEBRATE ZOOLOGY
INTRODUCTION
Tetrapods are direct descendents of a lineage of sarcopterygian fishes (Lab
6), and are diagnosed by several unique characters, many of which are
presumably adaptations to living in terrestrial environments. Among extant
tetrapods, Amphibia is the closest extant relative (CER) to Amniota (Fig. 6.1). In
lab 7, you will begin your examination of Amniota, inspecting representatives of
the reptilian clades Chelonia (turtles) Lepidosauria (emphasizing lizards and
snakes), and Archosauria (crocodylians and birds). Reptilians, through their
diverse taxonomic radiations, have successfully invaded land, water, and air.
Mammalia, the CER to Reptilia, will be presented in Lab 8.
In earlier taxonomies, Reptilia included Chelonia, Lepidosauria, and a
paraphyletic Archosauria (crocodylians and dinosaurs) that did not include
Aves (birds). Thus, Reptilia was paraphyletic and unacceptable. To rectify this
problem, Reptilia is definded as the most recent common ancestor of Chelonia,
Lepidosauria, Crocodylia, Aves, and all of its descendents; therefore, birds are
reptilians (Pough et aI., 1998, 1999). As already indicated, the term "reptiles"
has been used historically to refer to a paraphyletic group which includes all
reptilians except birds. To avoid confusion, we refer to the members of Reptilia
as reptilians and not as reptiles.
AMNIOTA
Amniota is diagnosed by numerous skeletal synapomorphies (Gauthier et
h'
aI., 1988), most of which will not be considered here. Three synapomorphies
which are readily observable at our level of analysis include the.amniotic egg.. ~1n!t0Ifla("f ~
modification of the second cervical vertebra into t];le ~, and the presence of:- / "~K.e hri
claws on the phalanges of fore- and hindlimbs. The amniotic egg consists of IPN.
three extra-embryonic membranes: the amnion, chorion, and allantois (Fig. 7.2).
In amniotes that are oviparous (i.e., egg laying), the egg has an outer, protective
covering termed the shell which is often calcareous (e.g., the cleidoic egg). In all
amniotes, the membranes of the amnion immediately surround the developing
embryo, which form a sac that is filled with amniotic fluid. The chorion serves
as a protective inner membrane lining the shell, and the allantois stores
metabolic wastes. Frequently, the chorion and allantois fuse to form a membrane
complex called the chorio-allantois membrane. The production of a shell-bound
egg necessitates internal fertilizati!J1J,; the males of mammals, turtles, and
squamates have independently evolved penis-like structures. In amniotes, the
second cervical vertebra, the axis, is modified from its ancestral condition to
allow sideways and rotary movements of the head. Claws are accumulations of
keratin that protect the terminal phalanx of the digits (Fig. 7.1) and are used for a
Lab 7: AMNIOTA: REPTILIA
179
Allantoic cavity
AMNIOTA
REPTILIA
Amnion
Amniotic cavity
(with amniotic fluid)
SAURIA
1LEPIOOSAURIA~[i
~
11
ARCHOSAURIA
~
U
ID
0
«
~
Embryo
(squamate)
'"
IhIJ--,HI--- Yolk membrane
Parthenogenesis
Hemipenes
'\2~~.-J~\-_
>
:J.c:o
&
Chorionic cavity _ _../1."':'0
Lateraiiy compressed tail
Feathers
Furculum
Pygostyle
Secondary palate
Synsacrum
Pneumatic bones
Keel on sternum
Keratinized bill
Teeth absent
TDSD absent
Dorsally place nostrils
Mammary
glands
Incus and
maleus
Heterodont
dentition
Teeth laterally compressed
Vocalization by territorial males
4 chambered heart
Yolk
Figure 7.2. Arrmiota: Amniotic egg of a squamate reptile, with the three extra-embryonic membranes, the
amnion (surrounding embryo), chorion, and allantois.
variety of functions, such as digging, defense, climbing, and courtship (Pough et
al., 1998, 1999).
Pre- and posthatch parental care (female and male)
Muscular, thoracic
diaphragm
Ql
Name at least two protective functions the eggshell might serve.
Q2
The calcareous shell ofa bird egg appears to be an impermeable barrier.
Nonetheless, a developing embryo obviously requires a continuous supply of
oxygen and the ability to remove carbon dioxide. What characteristics of the shell
might allow for gas exchange to occur?
Q3
Consider the evolution of the amniotic egg. What were some possible selective
agents for its origin and success?
Facultative bepedality
Single bone in lower
jaw (dentary)
Production of uric acid as an excretory product
Temperature-dependent sex determination (TDSD)
Hard (beta) keratin
Second cervical vertebra modified (axis)
Amniotic egg
Figure 7.1. Phylogenetic relationships of extant amniote clades. Modified from Pough et al. (1996).
180
LABS FOR VERTEBRATE ZOOLOGY
Lab 7: AMNIOTA: REPTILIA
181
Amniotes are diagnosed by other synapomorphies, including internal
fertilization and hard keratin covering the body. Keratin is produced in the
skin of all living tetrapods. The keratin in extant amphibians is very thin and
does not afford much protection against desiccation.
Peripheral series
(P1-P11)
Nuchal
Cervical
Pleural series
(P1-P4)
REPTILIAN DIVERSITY
...,.,.*-,~ Costal series
(C1-C8)
The extant species of Reptilia are represented by such clades as Chelonia
(turtles), Squamata (lizards and snakes), Sphenodon (tuatara), Crocodylia
(crocodilians), and Aves (birds) (Fig. 7.1). Reptilia is diagnosed by numerous
synapomorphies, including the Eroduction of uric acid as an excretory product,
color vision (color vision presumably evolved independently in some frogs,
some mammals, and Reptilia) and temperature-dependent sex determination
(TDSD), which, in brief, means that eggs incubated at specific temperatures
(e.g., high vs. low) develop as either males or females. As indicated,TDSD is
found in various chelonians, squamates, and probably all extant crocodylians
(Pough et al., 1998, 1999).
Vertebral
Series
A
Suprapygal
Pygal
B
CHELONIA
-'r--Gular
Chelonia (turtles) is currently recognized as the CER to Sauria (Fig. 7.1). A
recent study, however, argues that turtles may be the CER to Lepidosauria
(Rieppel and deBraga, 1996). Because this view is too new to be judged widely
among systematists, it is not adopted in this edition.
Examine a head skeleton of a turtle.
@
-""'...-- Epiplastron
--''r-
--+--4..--
Humeral
Entoplastron
Pectoral
Hyoplastron
!\:
Are teeth present? Is this condition derived or ancestral?
lib 5 el'1ff. of
-feefh
-~";:t. -
:::
~j~
:: Hypoplastron
--;:,'1~-~~.......,""'"".
Gastralia
Abdominal
.....
-+-- Femoral
Observe the emargination at the rear of the skull. This emargination,
which is unique to turtles, provides a greater area for jaw muscles to attach.
Other amniotes, such as mammals, lizards, snakes, and archosaurs have
temporal fenestrae, or openings in the sides of the skull, for muscle
attachment (Fig. 7.10). Ancestral amniotes lacked both temporal fenestrae and
the skull emargination possessed by chelonians.
182
LABS FOR VERTEBRATE ZOOLOGY
- " f - - Xlphlpiastron
c
+--Anal
D
Figure 7.3. Chelonia: Shell of turtle. (A) Dorsal view of the carapace (dermal bone). (B) Dorsal view of the
carapace showing the epide~mal scutes that overlay the dermal components. (C) Ventral view of the plastron
(dermal bone). (D) Ventral VIew of the plastron showing the epidermal scutes that overlay the dermal
components.
Lab 7: AMNIOTA: REPTILIA
183
Identify the first two cervical vertebrae, the atlas and the axis. Whereas the
head may move upward and downward on the atlas, the major component in
sideways and rotary movements of the head is movement of the atlas on the
axis.
Cervical vertebrae
.....
@ For which taxon is the presence ofan atlas a synapomorphy? The axis?
Radius
Ulna
""-ll"IT"'- Carpals
Turn your attention to the turtle sbelL which is a synapomorphy for turtles
(Fig. 7.3). The dorsal portion of the shell is the carapace. The ventral portion of
the shell is the plastron. The shell is composed of heavy underlying bony
plates, covered by epidermal scutes composed of keratin. Identify both dorsal
and ventral regions and their elements. For the most part, the boundaries
between the scutes alternate with the sutures between the bony plates, a
condition that lends strength to the shell structure as a whole. The three most
anterior bony elements of the plastron are actually the highly modified
clavicles (the epiplastron) and the interclavicle (the entoplastron). The other
plates are represented by gastralia, which are a series of dermal bones of the
abdomen ancestrally present in early tetrapods. Members of Crocodylia also
retain gastralia. The functional pectoral girdle is comprised of the coracoids
and scapula (Fig. 7.4).
Note also the condition of the vertebrae and ribs.
€V
What is the relation of the vertebrae and ribs to the carapace? How are they
positioned relative to the carapace? What functional advantages might this
condition offer?
-Phalanges
(with claws)
,
,
;
:,
Vertebra - - - - ' + .
Scapula
,"',
j
Coracoid
t. ....·;'
"....•
,;:-'''''-,-------i--
Pubis
.........
-i"-T----,'·"'··,--'f--Ischium
..... " ' ,
Femur --..;.,,.---'-;,,....""'_--
~~~'!l.~~::::::::::::,L-:::i--Ilium
Sacral vertebra
···,··,t" /,
.
i I
N...1-'n"J Tarsals
-Metatarsals
]
The ribs of turtles are unique among tetrapods in being external to the
girdles. Observe this condition. It remains a conundrum how this evolutionary
transition could have occurred.
Identify the specified bones of the turtle skeleton as indicated in Figures
7.3 and 7.4. You should recognize many of the bones from the lab on Amphibia
(Lab 6).
Observe the various preserved chelonians that are available to you. Find
the claws, which are present on the fore- and hindlimbs.
184
LABS FOR VERTEBRATE ZOOLOGY
Phalanges (with claws)
Figure 7.4. Chelonia: Ventral view of carapace illustrating the skeletal system of an emydid
(cryptodire) turtle.
Lab 7: AMNIOTA: REPTILIA
185
Q
U
For which taxon are claws a synapomorphy? Also, list several possible functions
offore- and hindlimb claws.
CHELONIA
CRYPTODIRA
PLEURODIRA
CHELONIOIDEA
TESTUDINOIDEA
Q)
til
"0
Note how different shell, head, and limb characteristics provide
information on how and where these species live (i.e., their ecomorphology).
Discuss this variation with your lab partners and instructor.
'>,
Qi
.s::
g
In each case how might the external morphology of the turtle indicate where and
how the animal lives?
Q)
til
32
Q)
til
32
c
'c 'g
E
.Q
Cl
o
Q)
Q8
TRIONYCHOIDEA
Q)
Q)
.s::
tl
Q)
f-
=Q)
til
"0
.<:
:J
Ol
j
=
Q)
til
"0
Q)
til
"0
'6
>-
'>,
Qi
.s::
()
0
:t::
til
"0
Ql
til
"0
:c
g,
~
til
"0
til
-
Ql
E
2
-E
Ql
E
UJ
A phylogenetic hypothesis for turtles is provided (Fig. 7.5). You may not
have access to preserved specimens representing all of the taxa represented in
the cladogram.
CHELONIAN DIVERSITY
There are ~ 250 species of extant turtles, 200 of which are members of the
clade Cryptodira. Cryptodires, including members of the clades Testudinoidea,
Trionychoidea, and Chelonioidea (Fig. 7.5), retract their heads into their shells
by bending their necks in a vertical S-shape. The remaining 50 species belong to
the clade Pleurodira (Fig. 7.5) (Pough et a/., 1998, 1999). The pleurodires are
collectively referred to as side-neck and snake-neck turtles because they retract
their heads by bending the neck laterally. Color illustrations of most species of
turtles are in Pritchard (1979), Stebbins (1985), Conant and Collins (1991), and
Cogger (1994).
Q9
.186
Refer to Chapter 12 in Pough et al. (1999). Describe the morphological differences
of the cervical vertebrae between the two major clades of turtles that permit
retraction of the head into the shell versus bending the neck horizontally. Under
what environmental conditions would the side-neck condition evolve?
LABS FOR VERTEBRATE ZOOLOGY
Figure 7.5. Phylogenetic relationships of tutle clades. Based on Pough et al. (1996.1999).
Pleurodira
The pleurodires comprise - 50 extant species distributed in two taxa
Chelidae and Pelomedusidae. Chelids (30 species) are found in South A~erica
as well as Australia and New Guinea. They include the side-neck turtles as well
as the bizarre and popular mata mata turtle. The pelomedusids (20 species) are
found In South AmerIca and Africa, and also are called side-neck turtles.
Lab 7: AMNIOTA: REPTILIA
.187
Cryptodira
Testudinoidea
Chelydridae
Testudinoidea is comprised of Testudinidae, Emydidae, and the
potentially paraphyletic "Bataguridae" (Fig. 7.5). The testudinids, commonly
called tortoises, comprise - 35 species of land-dwelling forms. Tortoises tend to
have highly domed shells and elephant-like hindlimbs. Some of them, such as
the Galapagos tortoise, are among the giants of turtles. The emydids comprise
the most taxonomically diverse clade of turtles with over 85 extant species, and
they range nearly worldwide. These are among the best known species, such as
box turtles, sliders, map turtles. Most species of emydids are amphibious.
Two species called snapping turtles (Chelydra and Macroclemys) are the only
members of this clade. Chelydrids are uniquely characterized by a long,
serpentine tail. Additionally, the plastron is cruciform in shape, the shell is
reduced in size, relative to most other turtles, and the neck is not completely
retractile within the shell (these additional character states are not unique to
chelydrids). Chelydrids are restricted to the New World (North, Central, and
South America). Both species have been, and remain, an important source of
food for humans. The alligator snapping turtle (Macroclemys temnicki) is
threatened in most areas of its range in the southeastern United States as a
result of over harvesting of adults.
Chelonioidea
Chelonioidea, which includes the sea turtles, is represented byCheloniidae and the monotypic Dermochelys (Fig. 7.5). Sea turtles have
paddle-like limbs which aid in swimming. Cheloniidae is represented by six
species that are distributed world-wide in marine habitats, both temperate and
tropical. The monotypic Dermochelys, the leatherback sea turtle, is the largest of
all turtles (nearly 2 meters in length) and can be found in a variety of marine
habitats, ranging from tropical to subarctic. Epidermal scutes and the bony
carapace are absent in leatherback sea turtles. Their shells are replaced by
leathery skin with isolated plates of bone.
Trionychoidea
Trionychoidea is comprised of Trionychidae, the monotypic Carettochelys
and Dermatemydys, and Kinosternidae (Fig. 7.5). The trionychids, softshell
turtles, comprise - 22 species occurring in North America, Asia, and Africa. In
these turtles, the shell is covered with undivided skin and a fleshy snout is
present. Members of Carettochelys are only found in New Guinea, and they
also have a shell covered with undivided skin, but there is no fleshy snout and
the carapace is reduced. Members of Dermatemydys occur in Mexico and
Central America. The kinosternids, called mud and stinkpot turtles, are
comprised of - 20 species found in North, Central, and South America.
Kinosternids have dome-shaped shells and many have plastrons with hinges
and barbels on the chin. These turtles often walk along the bottom of a stream
or pond and feed upon worms, snails, and other invertebrates.
188
LABS FOR VERTEBRATE ZOOLOGY
SAURIA
Sauria includes Lepidosauria and Archosauria (Fig. 7.1). Many saurians
are capable of facultative bipedality. Many members of this clade have front
limbs that are much shorter than the hind limbs, which is a retained, ancestral
character state. In some cases when a saurian begins to run fast, it rears its front
limbs off the ground and is able to run on its hind legs only. Since these species
are not obligated to run only on their hind legs, they are referred to as facultative
bipeds.
LEPIDOSAURIA
Lepidosauria includes Sphenodon, which is comprised of two species on the
off-shore islands of New Zealand, and Squamata, which includes a great
diversity (- 5700 species) of lizards and snakes (Fig.•7.6; Estes and Pregill, 1988;
Pough et al., 1998, 1999). Members of Sphenodon and many members of
Squamata (including several species of snakes) are capable of tail autotomy (a
synapomorphy for Lepidosauria). These taxa have a fracture plane through the
caudal vertebrae of their tails. When the tail experiences stress, it breaks
through one of the fracture planes. A new tail will regenerate, but it will not
have vertebrae; instead, it is replaced by cartilage. Perhaps you have attempted
to capture a lizard, only to have the tail wriggling about in your hand.
~
What are the possible functions for tail autotomy?
Lab 7: AMNIOTA: REPTILIA
189
LEPiDOSAURA
SQUAMATA
r - - - - IGJANIA
- - - , r - - - - - SCLEF03LOSSA - - - - - - , 1 1
SCINCOIVORPHA
Observe everted hemipenes in a preserved squamate (e.g., snake or lizard).
Look closely and notice the tiny spines on them (use a dissecting scope if
necessary). The position, number, and size of the spines are often used as
characters in systematic analyses.
AJ\GUIMORPHA
Qll
m
:Q
What might be the possible functions of hemipenial spines?
E
a;
J::
'"
m
:E
'"
0."0
o t::
"0
.~
c:
E '"0
>'"
~.3
Representatives of multiple squamate clades have been documented to
reproduce clonally by apomictic parthenogenesis ("virgin birth"). All-female
populations of various lizards, and members of at least one species of snake
(Ramphotyphlops braminus), reproduce without males (e.g., sperm is not required
to activate egg development nor is new genetic material incorporated),
producing female offspring that are essentially clonal to the mother (Pough et
aI., 1998, 1999).
@)under what environmental conditions would you suspect that parthenogenesis
evolved? What are the immediate advantages? Disadvantages? Is it present in other
amniote clades?
SQUAMATE DIVERSITY
Figure 7.6. Phylogenetic relationships among the extant lepidosaurians.1?e Resoluti:m of ~hyloge~etic .
relationships among non-acrodont iguanians remains elusive to systematlsts, Amphlsbaema an~ ~lbamldae
have been omitted from this cladogram due to their uncertain position within Scleroglossa, ModIfIed from
Pough et al. (1996,1999).
f",Me"c J ennjtl4,.";e,,,s
The two main clades of extant squamates'are Iguania and Scleroglossa
(Fig. 7.6). Iguania has 11 principal clades including the Acrodonta
(Chamaeleoninae + Agaminae + Leiolepidinae). Scleroglossa has four principal
clades including Gekkota, Scincomorpha, Serpentes (snakes), and
Anguimorpha. For various reasons, we did not include Amphisbaenia +
Dibamidae, member of Scleroglossa. Below is a brief description of several taxa
from Iguania and Scleroglossa that might be examined in this lab.
SQUAMATA
IGUANIA
Squamata includes all lizards and snakes (Figs. 7.1 and 7.6). A
synapomorphy for squamates is the presence of hemipenes i~ males. Th~se are
dual copulatory organs, and essentially they are equal to havmg two pemses.
During copulation, only one hemipenis is everted or extended from the base of
the tail and turned inside-out and is inserted into the female.
190
LABS FOR VERTEBRATE ZOOLOGY
Iguanian lizards are diverse in their morphology, and behaviors, but in
contrast to scleroglossans, none have evolved a limbless condition. Iguanians
are characterized by a fleshy tongue, an ancestral character state relative to
other squamates and to the tuatara, which is used to capture and manipulate
Lab 7: AMNIOTA: REPTILIA
191
food (Schwenk, 1994a, 1995; Cooper, 1996). Most iguanians are insectivores,
although a few, represented by the iguanids, are herbivores. Four of the major
clades are discussed below.
Iguanidae
Iguanidae is represented by - 31 species of which several are very familiar
to most, such as the Neotropical iguana (Iguana spp.), which is a common pet,
and the North American chuckwalla (Sauromalus spp.). Iguanids have colic
septa (septa in their colons) which are associated with their herbivorous diets.
®HOW might colic septa be advantageous to a herbivorous animal?
primarily in Africa (and countries to the north such as Yemen and Saudia
Arabia) and the island of Madagascar; several species also occur in Asia and
Europe. Chameleons possess several adaptations for arboreality, including a
long projectile tongue, zygodactylous feet, a laterally compressed body, eyes
which are stereoscopic, panoramic, and independent, and a prehensile tail.
Agamidae is taxonomically diverse and has over 300 species, including gliding
lizards of the genus Draco, frilled lizards (Chlamydosaurus kingii), and the
bizarre Moloch (Moloch horridus) which, in some respects, is morphologically
and ecologically convergent to horned lizards (Phrynosoma spp.) of the new
world. Leiolepididae is comprised of about 14 species that are herbivorous and
terrestrial, and found in Asia and Africa. Spiny-tailed lizards (Uromastyx spp.) are
among the largest of this clade, attaining lengths of nearly a meter. In some
respects, they are convergent to the New World chuckwallas.
SCLEROGLOSSA
Phrynosomatidae
This large lineage comprises over 117 species inhabiting North America, and
includes the famous horned lizards (Phrynosoma spp.) and the familiar and
common spiny or fence lizards (Sceloporus spp.).
Polychrotidae
Polychridae
This clade contains - 300 species in North, Central, and South America,
including the green anole (Anolis carolinenesis), the lizard misnamed as the
" American Chameleon." Most are arboreal, and a few terrestrial and aquatic
taxa occur in Central and South America.
~ If available, observe several anoles. How is the skin on their digits modified for
arboreality?
Scleroglossans are unique in that the vomeronasal organ (VNO)
(frequently called Jacobson's organ), paired chemosensory structures positioned
in the anterior nasal region, is more elaborate relative to other reptilians.
Correlated with this change, the tongue of scleroglossans is keratinized
anteriorly, and in several clades (e.g., Teiidae, Varanidae, Serpentes) has become
increasingly elongated and forked anteriorly (Schwenk, 1994a, 1995; Cooper,
1996). In fact, in these taxa, prey is captured exclusively with the jaws rather
than by the tongue (as in iguanians). Instead, the tongue functions as an
accessory organ for chemoreception by tongue-flicking. The tongue intercepts
molecules in the air or on the substrate, and upon retraction, the tongue and
other structures deliver the molecules to the epithelium of the VNO of the
anterior roof of the mouth. Snakes (members of Serpentes), of course, are
famous for tongue-flicking, but many scleroglossans also have forked tongues
and show frequent tongue-flicking regularly as well, especially teiids (e.g.,
members of Cnemidophorus) and anguimorphs (e.g., members of Varanus).
@
Why do snakes and somelizards have forked tongues? What is the utility ofa
anteriorly-bifurcated (forked) tongue versus one that lacks terminal forking?
Acrodonta
Gekkota
Acrodonta is composed of three main clades that include the familiar
and popular chameleons (Chamaeleonidae), with nearly 100 species found
Gekkota includes the familiar geckos (gekkonids and eublepharids) and the
less familiar pygopods. Geckos are abundant world wide with over 900 species,
192
LABS FOR VERTEBRATE ZOOLOGY
Lab 7: AMNIOTA: REPTILIA
193
and occupy a wide variety of temperate and tropical regions, as well as a wide
variety of habitats (Pough et al., 1998, 1999). Familiar species include the large
and highly vocal tokay gecko (Gekko gecko), the day geckos (Phelsuma spp.), and
the terrestrial leopard geckos (Eublepharis macularius). Convergent with
polychrotids, arboreal geckos have hook-like setae on the pads of their digits.
The pygopods (e.g., Lialis, Pygopus) are unusual in that they are snake-like in
appearance (e.g., body serpentine, no eyelids, absence of forelimbs and pectoral
girdles), but some have external ear openings and conspicuous hindlimb flaps
near the vent. The -36 species are restricted to Australia and New Guinea
(Cogger, 1994; Pough et a/., 1998, 1999).
Scincomorpha
Scincomorpha is represented by eight distinctive taxa (Fig. 7.6). Several of
these lineages are Scincidae (over 700 species), Teiidae (- 80 species),
Lacertidae (-150 species), and Cordylidae (- 42 species). Scincids, are found
worldwide and show amazing morphological and ecological diversity. Scincids
are diagnosed by the presence of cycloid scales. Also, they are generally
fusiform with small, short legs, and they have tails which are not particularly
distinct from their bodies. Teiids are restricted to the New World and include
species such as the whiptails (Cnemidophorus spp.), some of which are
parthenogenetic (virgin birth), and the large tegus of South America
(Tupinambis spp.). Lacertids are distributed in the Old World, and include the
common terrestrial species of the genus Lacerta. Cordylids are restricted to the
sub-Saharan regions of Africa and are primarily rock-dwelling. The sungazer
(Cordylus giganteus) is one of the largest cordylids.
Amphisbaenia
Amphisbaenia is an unusual lineage of lizards collectively referred to as
amphisbaenans, and is composed of three main clades with - 133 species
distributed worldwide. Most lack limbs and are fossoria!. Understandably, due
to their secretive nature (i.e., fossorial), little is known of their natural history.
Due to uncertainties of their exact position in Scleroglossa, amphisbaenans, as
well as the rarely observed dibamids (- 9 species; New- and Old Worlds), are
not presented in the c1adogram in Figure 7.6 (see Pough et al., 1999).
SERPENTES
Many studies indicate that Serpentes (snakes) is a monophyletic taxon of
the Scleroglossa and the CER to Anguimorpha, with similarities to members of
Varanoidea which includes monitors (Varanus spp.) and two species of beaded
lizards, Heloderma (Fig. 7.6) (Pough et a/., 1998, 1999). Color illustrations of many
species of snakes can be found in Stebbins (1986), Conant and Collins (1991), as
well as Shine (1991) and Greene (1997).
(~nD Does this mean that lizards, as typically defined, form a monophyletic group?
Anguimorpha
Why?
Anguimorpha is comprised of four distinctive taxa (Anguidae,
Xenosauridae, Heloderma, and Varanidae), and it is the CER to Serpentes,
which includes all snakes (Fig. 7.6). All anguimorphs have a tongue in which
the foretongue retracts within the hindtongue at a zone of invagination.
Anguidae includes alligator lizards (e.g., Elgaria), legless, burrowing lizards
(Anniella), legless, terrestrial lizards (Ophisaurus), and others. Heloderma is
comprised of two species, the gila monster and the beaded lizard; these are the
only venomous species of lizards and both occur in western North America,
and the beaded lizard reaches western Central America. The two species of
Heloderma have grooved, venom-conducting teeth on the mandibles (lower
194
jaws). There are - 40 species representing Varanidae. Varanids have several
modifications of the skulI which contribute to its highly kinetic nature and
carnivorous diet. The best known and perhaps the most famous of the varanids
is the Komodo dragon (Varanus komodoensis), which inhabits Komodo Island
and several others nearby, and it is the longest and heaviest of extant lizards.
All varanids are distributed in the Old World.
LABS FOR VERTEBRATE ZOOLOGY
SNAKE DISSECTION
External Morphology
As an exercise to better understand the specializations of snakes and
vertebrate homologies in general, your instructor will provide a preserved
Lab 7: AMNIOTA: REPTILIA
195
snake. Examine the dorsal anterior region first. Observe that the eyes have
transparent, fixed eyelids. This character is present in all snakes (modified in
some basal taxa), but is also present in taxa of lizards, such as some species of
gekkotans. Just posterior to the eyes note that external ear openings are
absent. Again, all snakes lack external openings to the ear, but this character
state is also present in some taxa of lizards (e.g., chameleons and several
limbless, fossoriallizards). If you have a pitviper, boa, or python to examine,
find the external pits of the facial scales that lead to the infrared organs. The
dorsal scales of snakes are not contiguous (i.e., connected to each other) but
rather separated by interstitial tissues. Dorsal scales can vary greatly in size,
and be either smooth or keeled.
Position your specimen on its dorsum to view the venter. Note that the
ventral scales are larger than those of the dorsum, and that they tend to be flat
and smooth. Depending on the taxon, ventral scales vary in size and number.
Move to the posterior region. If you have a boid or pythonid snake, locate the
vent region and observe the pelvic spurs, which are vestiges of the hindlimbs
(vestiges of the pelvic girdle are internal, of course). These spurs can show
sexual size dimorphism and, in general, are larger in adult males than in
females, and males use pelvic spurs in courtship to stimulate females to mate;
there is no known function of the spurs in females.
Heart
Thymus
lung (left)
Posterior tongue
Trachea
-='"'l;;=-- Stomach
Gall bladder
L~~~~~Spleen
-ff-- Hemipenis
-'-'11.......-
Pancreas
Internal Morphology
Make an incision from the mouth to the cloaca (Fig. 7.7). Starting from the
anterior region, locate the posterior tongue, trachea and single functional
lung.
Q17
®
(;.Q(!e.-
01,
J0ti,.-
50
Small intestine
Anal scale (divided)
~ • • , • • • • --"<,
.........
Where is the anteriormost region of the trachea located? Is it in the buccal
cavity? Why?
Why do most snakes only possess a single functional lung? Which lung (left or
right) is vestigial?
/./::#--J!j'---
.'\
Kidney (left)
Ductus deferens
."
Adrenal (left)
~ !,
J'".te5 5«';0
I~
M.,.n.
Figure 7.7. Serpentes: Internal anatomy of a harmless (colubroid) snake (male).
A>-...i'",
@,"os
I",v( (0.5";,, ~0".5 ....;- .,10.,... 1 s/-Y'pe5
(!) ,,",,,I IJIJgr"I't I of ~b;t~f.s At S~A ..", .-..glA"!f4i,,f
(!!)'~"'A-/;'. re",i .• ~",.hc, .r /<"<.d"'A/
(ff) ,.fi-prr.!"fo.,. ~"VD;J i.e •.> .... {!I<f.t I1'>lAs/r.
@- Ji"t·h'('6V;~
196
LABS FOR VERTEBRATE ZOOLOGY
Lab 7: AMNIOTA: REPTILIA
197
In the region of the posterior trachea, locate the thymus, thyroid, and heart
(ventricle and atria). Both the thymus and thyroid are endocrine glands. Return
to the mouth and trace the esophagus to the stomach, continuing to the small
intestine and large intestine.
Q19
Examine the skeletal material available and refer to Fig. 7.8. Observe
closely the size and position of the bones of the head skeleton, including the
mandible (lower jaw).
What properties of the stomach permit snakes to consume large prey?
In the midbody region, locate the liver and gall bladder (and bile duct).
The pancreas and spleen are located posterior to the liver and gall bladder and
are often adjacent to each other. Just anterior to the vent (opening to the cloaca),
locate the paired, elongated kidneys (composed of about 25 lobes). The paired
gonads of both sexes are located just posterior to the region of the liver and gall
bladder. The testes are elongate and asymmetrically aligned, and sperm are
transported via the ductus deferens to a hemipenis, each of which is located in
the tail. Each testis is individually connected to a hemipenis; thus, snakes (and
lizards) have a dual (i.e., separate and independent) delivery system for male
gametes.
Q20
Skeletal System
What might be the adaptive significance of hemipenes and a dual gamete
delivery system?
Q22
Based upon your observations, how can a snake swallow a meal larger than its
head? What bones are most important in accomplishing this feat? Compare the
mandibles of a lizard to that of a snake. How do they differ?
Q23
What postcranial elements permit snakes to have an extremely flexible vertebral
column? What would be the possible selective agents for the evolution of this
specialization? What is the current utility of vertebral flexion?
Q24
Ribs are present on nearly every vertebra in snakes. What are their functions?
FEEDING SPECIALIZATIONS OF SNAKES
The ovaries are larger but less descript than the testes. In both oviparous
(egg-layers) and viviparous (bearers of fully developed young) taxa, mature
ova are transported from the ovary to the oviducts. Oviparous taxa possess
shell glands that cover the ova, and the mature shelled-eggs are expelled
(oviposited) through the cloaca, and all subsequent development occurs
outside the female's body. Development in viviparous taxa occurs entirely
within the oviduct, and parturition does not occur until development is
completed.
Q21
198
For which taxon do you think shell glands may be unique?
LABS FOR VERTEBRATE ZOOLOGY
All snakes (-2500 species) are carnivorous, and all must capture and
subdue their prey. Essentially, there are three principal modes of prey capture:
overpowering prey, constricting prey, and envenomating prey. Although
these modes are not necessarily mutually exclusive, there is rarely overlap.
Several lineages of snakes possess a venom delivery system (venom
glands, venom, venom ducts, and enlarged teeth called fangs which are
hollow or grooved). The most notable venomous species are the members of
Elapidae (e.g., cobras, mambas, seasnakes, and relatives) and Viperidae (e.g.,
vipers and pitvipers) (Pough et al., 1998, 1999). The elapids have relatively small,
fixed (somewhat fixed) fangs (proteroglyphs). The viperids have large,
retractable fangs (solenoglyphs). Another group of venomous taxa, collectively
called rear-fanged snakes, a group which is not monophyletic, have either hollow
Lab 7: AMNIOTA: REPTILIA
199
Postorbital
Prefrontal
Nasal
Supraoccipital
Frontal
Maxilla
Postorbital
Maxilla
Premaxilla
(with teeth)
Prefrontal
Frontal
--.,..t
Prootic
Supraoccipital
Supratemporal (squamosal)
"V1'""'!"","'l;;~~~_ Exoccipltal
Premaxilla
",,~~=-:Q~Uadrate
'"
Stapes
_-i~~~
Basioccipital
FangProotic
Ectopterygoid
Coronoid
Angular
Dentary
Mandible [
Compound
(with articular)
A
Dentary
Maxilla
Compound (with articular)
c
Nasal
Prefrontal
Frontal
&'1'>._- Postfrontal
Palatine
Ectopterygoid
a",,_- Parietal
"."r-- Supratemporal (squamosal)
~:'ii'fl--- Prootic
Basisphenoid
Postorbital
Parasphenoid
Stapes
Supraoccipital
Pterygoid
Supratemporal (squamosal)
Quadrate
Basioccipital
",,-.,-- Quadrate
Premaxilla
-<~j~"~~~
Compound (with articular)
B
Dentary
Dentary
Figure 7.8. Serpentes: Head skeletons of a (A) pythorid snake, nonvenomous (African rock python, Python
sebae), (B) viperid snake venomous (red rattlesnake, Crotalus exsul), (C) elapid snake venomous (green
mamba, Dendroaspis viridis), and a (D) rear-fanged snake venomous colubrid (boornslang, Dispholidus typus).
200
LABS FOR VERTEBRATE ZOOLOGY
Compound (with articuiar)
D
Lab 7: AMNIOTA: REPTILIA
201
or grooved fangs in the rear of the mouth (opisthogylphs), and include such
members as the boomslang, Dispholidus typus (Fig. 7.8). In all species, the fangs
are located on the maxilla of the upper jaw, and they are replaced regularly. The
venom glands are located on the dorsal-lateral aspect of the head, posterior to the
eyes. Examine the head of a preserved elapid or viperid and identify the fangs
and location of the venom glands.
~ Can you identify any selective advantages to having rear fangs?
Most boas (Boidae) and pythons (Pythonidae) have infrared receptor
organs (heat-sensitive organs), which are visible on the external body as
depressions or pits of the face scales (e.g., labial or loreal scales). Similar organs
(and pits) have evolved independently in pitvipers (members of Viperidae).
World) have a suite of morphological adaptations for arboreality. These include
prehensile tail that lacks autotomy, laterally compressed body, opposable
digits (zygodactyly), eyes capable of independent movement, and elongated
and protractable tongue.
@
How would each of these morphological modifications be adaptive for
arboreality? Can you identify more characters?
Many species of geckos, members of Gekkonidae, also have evolved
features for arboreality. Note the condition of the digits on a representative
arboreal gecko. Examine them closely under a dissecting microscope.
Q28
Explain how this gecko's morphology may be adaptive for arboreality.
~ What type(s) of prey would the infrared organs be useful for detecting? Do you
C:.J think they might have other functions?
ECOMORPHOLOGY OF SQUAMATES
As you learned in Lab 6 (Amphibia), one can make reliable predictions of
the life habits of an organism on the basis of its overall morphology. As in
Amphibia, the same comparisons and predictions can be made in squamates.
Here, for time considerations, we shall restrict the coverage to lizards.
1. Amphibious. Lizards that dwell near lakes, streams, and oceans. They often
enter the water to forage or to avoid enemies. Enemy avoidance is particularly
notable in the basilisk lizard (Corytophanidae: Basiliscus spp.) which can run
bipedally atop the water for short distances when chased. Morphological
features indicative of amphibious habits include a long, powerful laterally
compressed tail which is used as a locomotor organ. Another example is the
crocodile lizard (Xenosauridae: Shinisaurus crocodilurus) of China.
2. Arboreal. Lizards that climb trees, shrubs, or rocks. For example, the
extremely popular true chameleons, members of the Chamaeleonidae (Old
202
LABS FOR VERTEBRATE ZOOLOGY
3. Generalized terrestrial. Lizards that are active on the surface of the ground
to forage for extended long periods, but will hide beneath logs, rocks, and the
like. In generat, they possess no specific set of characters for the habitats they
lIve. Examples mclude sideblotched lizards (Uta spp.), whiptails
(Cnemidophorus spp.), and the desert iguana (Dipsosaurus dorsalis).
4. Strictly fossorial. Limbless or nearly limbless lizards that occupy subterranean
habitats. These lizards spend extended periods beneath the surface of the
ground, and often construct extensive burrows. Fossoriallizards generally have
reduced eyes, countersunk lower jaw, and a tympanum is usually absent.
Examples include the California legless lizard (Anguidae: Anniella pulchra),
amphisbaenids (member of Scleroglossa), and many scincids (Scincidae).
5. Grass swimmers. Generally limbless lizards, but some with small, reduced
limbs that occupy leaf litter or dense vegetation, such as fields. They are similar
to other lizards in most respects (e.g., they possess well developed eyes,
tympanum present), except grass swimmers are limbless or have very reduced
limbs with relatively long tails and serpentine bodies. Examples in North
America include the glass lizards (Anguidae: Ophisaurus spp.) and many
scincids (Scincidae).
Note the diversity of other lizards available to you. Pay especial attention
to those taxa that are legless or show limb-size reduction. Compare them to
any available species of snake.
Lab 7: AMNIOTA: REPTILIA
203
~
ARCHOSAURIA
What character(s) is (are) definitive in separating lizards from any snake?
CROCODYLIA
C;OCODYLlDAi1i;AVIALIDAE
ARCHOSAURIA
Archosauria includes Crocodylia and Aves (Fig. 7.1; Benton and Clark,
1988; Gauthier et aI., 1988; Kemp, 1988; Schultze and Trueb, 1991). Aves is a
member of the stem clade Dinosauria, which also includes extinct taxa such as
the familiar Apatosaurus, Tyrannosaurus, Stegosaurus, Deinonychus,
andVelociraptor Fig. 7.9, Pough et aI., 1999). Synapomorphies of the Archosauria
include a four-chambered heart, presence of a gizzard (which is a modified
portion of the anterior stomach), pre- and posthatch parental care (female or
both sexes), vocalizations by males to defend territories and attract mates,
fore- and hindlimbs beneath the body instead of out to the sides (sprawled) as
in other reptilians (the position of the legs permits archosaurs to breath while
they run), elongation of the pubis and ischium (pelvic girdle components),
reduction or absence of fifth toe, laterally compressed teeth, and an
antorbital fenestra (Gauthier et aI., 1988; Kemp,1988; Shine, 1988).
r~8
o
<'3
1~
~L~
.!!;!
~112
8~
~~
0
2
E
.~
:s
~
:.:::::
ALLIGATORIDAE
l
~
CROCODYLIA
Crocodylians first appeared in the Triassic and include the extant
crocodiles, alligators, caimans, and gavials. Crocodylians differ from all other
reptilians in having a secondary palate, which fully separates the nasal
passages from the oral cavity (Fig. 7.10). Beneath the original palatal roof, the
maxillary, palatine, and pterygoid bones have built a secondary shelf or palate
of several bones. Between the braincase and this underlying shelf, canals run
back from the dorsally placed external nares to open into the mouth far back,
above the opening to the trachea. A flap of skin just in front of this point can
close off the pharynx from the mouth so that breathing can be accomplished
underwater, even with the mouth open, provided that the external nares are
exposed above the surface.
c9
204
Describe the ecological significance of the secondary palate. What does it permit
crocodylians to do that other reptilians cannot?
LABS FOR VERTEBRATE ZOOLOGY
Figure 7.9. Phylogenetic relationships among crocodylians. Note that Aves is the CER to Crocodylia.
Modified from Poe (1996).
If preserved crocodylians are available, observe the laterally compressed
tail and webbed feet, two adaptations to an aquatic existence.
Lab 7: AMNIOTA: REPTILIA
205
Q
,...--- External naris
'r--';-'".-e"r- Anterior palatine foramen
-,,':"fir-- Premaxilla
- - - Premaxilla
(tooth-bearing)
Nasal
>:~-~'iI--
Maxilla
Maxilla
(tooth-bearing)
southeastern United States, and the Chinese alligator (A. sinensis) which occurs
today in the lower Yangtze River basin in China. Both species of alligators have
broad snouts relative to crocodiles and gavialids. There are six species of
alligatorids called caimans (Caiman and Paleosuchus), and all are from the
Neotropics, from Mexico to South America.
Q31
How can you explain the disjunct distribution of the two species of Alligator?
-tF-'4!"'4---- Palatine
- - - Lacrimal
Crocodylidae
~--Jugal
44+-- Frontals
.;.c.;f'I--- Ectopterygoid
(fused)
'l-__ Jugal
.:.;A,--- Internal naris
Postorbital
(,4"'1-++-- Basisphenoid
'4l,...-- Parietals
(fused)
+-'r-- Basioccipital
Squamosal
;,L,\''<'I-- Quadratojugal
Quadratojugal
Quadrate
A
There are 13 species of crocodiles (Crocodylus and Osteolaemus) which are
distr.ibuted in both.New and Old Worlds. Crocodiles are generally the largest
speCies of crocodyhans and those most likely to attack (and consume!) humans.
The most dangerous include the saltwater crocodile (c. porosus) and Nile
crocodile (c. niloticus).
Q32
If you have multiple species for comparison, can you detect what morphological
differences of the head skeleton separate alligatorids from crocodylids? (Hint:
look at aspects of the tooth arrangement.)
,:.cc"'iii!8-- Quadrate
B
Figure 7.10. Archosauria: Head skeleton of an American alligator (Alligator mississipiensis). (A) Dorsal and
(B) ventral views.
CROCODYLIAN DIVERSITY
There are 23 species of extant crocodylians in three distinct clades:
Alligatoridae, Crocodylidae, and Gavialidae (Fig. 7.9) (Poe, 1996).
Crocodylians occur primarily in tropical regions; however, several species are
found in subtropical and temperate environments (Pough et aI., 1998, 1999).
Gavialidae
The two extant. species of gavialids are the Tomistoma or false gavial
(Tomlstoma schiegelll) and gavial (Cavialis gangeticus). Both are very similar in
appearance, having extremely slender snouts. The gavial is restricted to rivers
(e.g., Ganges) in India and nearby countries (Nepal, Pakistan), and the
Tomistoma occurs in Indonesia and Malaysia, but its exact distribution remains
to be described.
CROCODYLIAN SKELETON
Alligatoridae
There are eight extant species of alligatorids. The genus Alligator has two
species: the American alligator (Alligator mississipienensis) which occurs in the
206
LABS FOR VERTEBRATE ZOOLOGY
Because of the difficulty in obtaining whole specimens of young preserved
crocodyhans, only skeletal elements will be presented. Examine a mounted
articulated skeleton of a juvenile crocodylian, probably an American alligator
Lab 7: AMNIOTA: REPTILIA
207
(Alligator mississipiensis). Locate and learn the head skel.eton (skull and
.
mandible), hyoid, atlas, axis, cervical vertebrae, thoracIc vertebrae (and n?s),
lumbar vertebrae, sacral vertebrae, caudal vertebrae, ilium, ischium, pUbIS,
scapula, procoracoid, humerus, radius, ulna, c~rpals, met~c~rp~ls,
episternum, sternum, costal cartilages, gastraha, femur, tIbIa, fIbula, tarsals,
metatarsals, and phalanges (fore- and hindlimbs).
~ For which taxon are the hyoid,atlas, humerus, radius, ulna, sternum,femur,
~ tibia, and fibula synapomorphles?
which are related to flight. Some of these also are shared with A. lithographica or
even other coelurosaur or theropod dinosaurians. Relative to other extant
amniotes, avian synapomorphies include the feathers, keratinized bill, keeled
sternum, clavicles fused to form a fmculum, pneumatic bones, reduction and
loss of forelimb bones, fusion of numerous vertebrae to each other and to the
pelvic girdle (synsacrum), re-orientation of the pelvic bones, reduction of the
fibula, fusion of tarsals to the tibia (tibiotarsus), fusion of metatarsal bones
(tarsometatarsus), loss of the fifth digit on the hindlimb, and reduction of
caudal vertebrae to a pygostyle (Fig. 7.1). These synapomorphies and their
functions will be discussed below.
AVIAN DIVERSITY
/Q34)For which taxon is the axis a synapomorphy? What are the functions of the
~axis?
(§
Q36
Struthioniformes includes the ostrich, rheas, emus, kiwis, and others. These
birds are flightless.
What are gastralia?
How are cervical, thoracic, lumbar, sacral, and caudal vertebrae distinguished?
Anseriformes includes about 150 species of ducks, geese, and swans. These
birds have broadened bills containing many tactile nerve endings and filtering
ndges at the margins. Their legs are short and their feet are webbed. Their
bodies are covered with many down and oily feathers. The young of
anseriforms hatch in an advanced state, capable of walking, swimming and
feeding on their own; they are considered precocia,!.
Passeriformes includes over 5,000 species of so-called perching or song birds,
IncludIng wrens, swallows, flycatchers, sparrows, thrushes, warblers, crows, and
many others. The young of all passeriformes hatch naked, blind, and helpless;
they.are considered altricial. The syrinx, a tracheal structure unique to birds, is
relatIvely complex in passeriforms, thus allOWing a complexity of song types.
AVES
Birds are descendants of a group of small theropod dinosaurs called
coelurosaurs (Gauthier, 1986). The earliest known birds are fossil
representatives of Archaeopteryx lithographica which have been found in strata of
Jurassic origin (- 160 million years old). Extant lIneages of bIrds are members
of the crown clade Aves, which includes the most recent common ancestor of
all extant birds and its descendants. Individuals of A. lithographica retained
many ancestral reptilian characters, including a long tail, many small teeth,. and
claws on their forelimbs. Extant birds share numerous aVIan synapomorphles
208
. Birds are taxonomically diverse with more than 9,700 described species
dlstnbuted throughout numerous distinctive clades (Fig. 7.11; Welty and
Baptista, 1988; Feduccia, 1996). Below we provide a relatively brief overview of
the taxonomic diversity of relatively familiar and popular birds.
LABS FOR VERTEBRATE ZOOLOGY
Piciformes includes over 205 species of woodpeckers, toucans, and others.
Many woodpeckers have greatly extensible tongues which is made possible by
the elongation of the hyoid bones.
Strigiformes includes over 150 species of owls. These are largely nocturnal
predators with large, forward-directed eyes set in feathered disks; large
external ear openings with flaps; short, powerful, hooked beaks; strong feet
WIth sharp talons; and soft, fluffy plumage that allows silent flight.
Lab 7: AMNIOTA: REPTILIA
209
ARCl-OSAURIA
AVES
Psittaciformes includes over 350 species of lories, parrots, and macaws.
Psittaciforms have narrow, hooked beaks with the upper mandible hinged to
the skull. Many species possess brilliantly colored plumage.
Charadriiformes includes over 350 species of shore birds, gulls, terns,
sandpipers, avocets, and others. Some charadriiforms are specialized fish eaters
(e.g., terns), others have specialized bills used to probe in the sand or mud for
invertebrates (e.g., avocets), and gulls are rather generalized carnivores.
Columbiformes includes over 300 species of doves and pigeons, as well as the
extinct dodos. These birds have relatively short and slender bills, short necks,
and short legs. Females produce "pigeon's milk" _ an energy and nutrient
rich, creamy fluid - in their crops to feed their young.
Falconiformes includes over 290 species of falcons, eagles, hawks, vultures,
and the osprey. Falconiforms are diurnal birds of prey with strong, hooked, and
sharp-edged bills; sharp, curved talons on the feet; and extremely keen vision.
Apodiformes includes over 430 species of swifts and hummingbirds. These are
relatively small birds with short legs and small feet, and their bills are either
small and weak (swifts) or long and slender with tubular or brushy tongues
(hummingbirds). Not only can hummingbirds hover, but they also can fly
backwards. Hummingbirds feed on flower nectar as well as small insects.
Pelecaniformes includes over 60 species of pelicans, boobies, cormorants,
frigate birds, and others. These birds are largely diving fish eaters along coastal
and offshore areas of oceans. Their toes are unite~ in one web, they have long
beaks with nostrils rudimentary or absent, and they possess throat pouches
(except in the species of tropic birds).
Sphenisciformes includes about 18 species of penguins which are distributed
around Antarctica and cold waters as far north as the Galapagos Islands.
Penguins' wings are modified into thin, powerful paddles and they have scalelike feathers.
.
..
extant birds. This cladogram, proposed by .Mindell (Tree of
F
igure 7.11. Phylogeneltc relatIOnshIps among
d'
fb' d elationships includmg Cracraft (1988),
Life 1997) represents a consensus amang three recent stu les 0 If r
.
Sibl~y and Alquist (1990), and Minden et al. (1997).
DISSECTION OF ADULT PIGEON
External Morphology
Obtain a preserved rock dove (Columba fasciata) from your instructor. An
important synapomorphy of birds is the presence of feathers.
210
LABS FOR VERTEBRATE ZOOLOGY
Lab 7: AMNIOTA: REPTILIA
211
@
What structures of other reptilians might be homologous to feathers? How could
you test your hypothesis?
-'1-
Pennaceous
region
Vane
It has been hypothesized that feathers had their origin as an insulating
device. Birds are endothermic (i.e., they produce significant heat through
metabolic activities), and some evidence points to several dinosaur relatives as
being endothermic, although this hypothesis remains controversial.
Feathers (Fig. 7.12) are well-developed and generally cover the entire body.
Ornithologists typically distinguish five types of feathers, including (1) contour
feathers, (2) semiplumes, (3) down feathers, (4) bristles, and (5) filoplumes
(Pough et ai., 1999). In contour feathers, a central rachis bears closely spaced
side branches called barbs. The barbs on either side of the rachis constitute a
surface termed a vane. Barbules, located on the barbs, are hook-like structures
arranged so that the feather remains strong and intact for flight. If the feather is
disrupted, preening behavior realigns the barbules. Countour feathers are
found on the body, wings, and tail. Down and semiplume feathers have soft or
downy barbs, and both types provide insulation to the bird. Filoplumes are
fine, hair-like feathers with a few short barbs or barbules at the tip. Free nerve
endings of filoplumes sense changes in pressure and vibration, and as such,
they can transmit information about the position and movement of the contour
feathers. Bristles are specialized feathers with a stiff rachis and barbs either
present or absent on the very tip. Bristles are usually found around the eyes
and on the head or on the toes. These feathers screen out foreign particles from
the nostrils and eyes and act as tactile sense organs.
Identify the various feather types using the pigeon, any preserved bird
skins available to you, or through the inspection of isolated feathers removed
from birds.
Study an isolated flight feather from the distal portion of a wing as an
example of a typical feather. Dry off the feather by blowing on it, but do not rub
it with a paper towel. Remove a small portion of the vane and observe it under
a microscope. Notice the smaller barbules that are set at an angle to the axis of
the barb. The barbules themselves may have smaller barbicels connected to
them, some of which may be hook-shaped (Pough et ai. 1999).
Find the uropygial (oil) gland on the ventral surface of the pygostyle.
'S4:~-- Plumulaceous
region
Vane
B
Vane
(plumulaceous)
Ifl--- Calamus
c
A
Rachis
i~f~~~;i~~~ves:
LABS FOR VERTEBRATE ZOOLOGY
(-1-'-- Calamus
Rachis
o
212
11--- Calamus
Rachis
Internal pulp cap
of calamus
Types of feathers.
Lab 7: AMNIOTA: REPTILIA
(A)
E
Calamus
Contour (remex). (B) Body contour. (C) Semiplume.
(0)
Bristle.
Flight feather
213
~ Birds may preen (groom) their feathers up to 20 times a day. What do you think
CJ the functions of this behavior are?
Buccal cavity
Facial muscles
Esophagus ---1
++-- Trachea
Internal Morphology
Open and examine the mouth of your pigeon (Fig. 7.13). In birds, teeth
have been functionally replaced by a keratinized, epidermal sheath (the beak).
Look into the mouth and find the opening to the esophagus and locate the
glottis, the anterior-most opening of the trachea.
e
Heart
Liver --b--_+_-
How do birds prevent food from entering the glottis?
Gizzard
Kidney
Fig 7.13. Internal anatomy of a pigeon (columba).
+-- Heart
Using strong scissors and/ or a sharp scalpel, cut the large breast muscles
from the area of the sternum to reveal the internal viscera. Continue your
incision through the throat region to reveal the esophagus and trachea (Fig.
7.13). You will have to cut through and remove the keeled sternum, a bony
element that allows for extensive muscle attachment.
e
I
J"g..J,.-- Proventriculus (anterior stomach)
Liver (left)
Liver (right)
What organs does the trachea lead to?
Gizzard (posterior stomach)
Small Intestine
Find the heart, remove the pericardial sac, and identify the four chambers
(right and left atria, right and left ventricles). The four-chambered heart is a
synapomorphy for CrocodyIia and Aves (Archosauria).
Find the crop, liver, lungs, gizzard, kidneys (three irregular lobes),
stomach, and small intestine (Fig 7.13 and 7.14).
~:7·r+-- Duodenum (loop)
t: cl'--- Oviduct
Colic
Caeca
Coprodaeum
Figure 7.14. Internal anatomy of a pigeon (Calumba).
214
LABS FOR VERTEBRATE ZOOLOGY
Lab 7: AMNIOTA: REPTILiA
215
~ What might be the function(s) of the crap and gizzard, taking into account their
~ relative position and contents?
-
Phalanx 2 (Digit 3)
~-- Phalanx 1 (Digit 3)
n'---~ Phaianx 1 (Digit 4)
.- . -. ~
Note the size of the heart and the compact nature of the internal organs.
The lungs are actually connected to numerous, paired, interconnected pouches
that allow continuous flow of air through the lungs. (Pough et aI., 1999)
- - Metacarpals (2-4)
(Carpometacarpus)
"-.'
Ulnare
Uina
Cervical
vertebrae
Scapuia
ilium
Caudal vertebrae
Thoraic
Skeletal System
vertebra
Using a reconstructed (articulated) pigeon (or chicken) skeleton, identify
the labeled bones and other elements (Fig. 7.15).
Several skeletal features of birds are associated with flight (Romer and
Parsons, 1986; Feduccia, 1996). The skull has been lightened by having no teeth
(tooth function has been replaced by a beak made of keratin).
The pectoral girdle has been modified to accomodate the extremely high
stresses experienced while flapping the wings. The energetic thrust of each
beating wing in transferred to the body through three bones of the pectoral
girdle, scapula, coracoid, and clavicle, with one set on each side of the ribcage.
The clavicles actually are fused to form the furcula (wishbone). The scapula is a
thin, blade-like bone along the side of the vertebral column. Interposed
between the wing muscles and the ribs, the scapula, along with the furcula,
braces the shoulders against the dislacements caused by the flapping motion of
the wings. The stout coracoid bone braces the sternum against the powerful
compression created when the chief breast muscles contract to cause the
downbeat of the wings. The two halves of the shoulder girdle are united in
front by the V-shaped furcula. It serves as a strut to brace the two wings apart.
Limbs, as well as some portions of the skull, are lightened by
pneumatization of bones (so-called hollow bones). Many of the resulting
spaces are filled with respiratory extensions of the air sacs connected with the
lungs.
Synsacrum
Coracoid ---H-',-'\
Ciavicie (furculum)---o,\
~':."±'e;;:-- ilioschiatic foramen
Rib
(with unicate process)
.:-;;"--Ischium
Sternum --".L-._ _
Femur
Keel (carina) --'~
Fibula (not shown)
\A,--Tibiotarsus
/r--Tarsometatarsus
Phalanges
~ Would pneumatization of banes make the skeleton mare fragile? Why or why nat?
Figure 7.15. Aves: Skeletal system of a pigeon.
21.6
LABS FOR VERTEBRATE ZOOLOGY
Lab 7: AMNIOTA: REPTILIA
217
The vertebral column is rigid due to the fusion of numerous vertebrae. As
in many other tetrapods, several regions of the vertebral column are
distinguished, including the cervical, thoracic, lumbar, sacral, and caudal. In
birds, many of the vertebrae are fused together to provide a light and stiff
framework. The sacral vertebrae are fused with lumbar vertebrae in front and
a few caudal vertebrae to the rear to make a rigid plate of bone, the
synsacrum. The synsacrum has also expanded laterally to fuse with the pelvic
bones.
The pelvic bones are significantly modified in size and orientation.
Ancestrally, the pelvic bones (ilium, ischium, and pubis) radiated outward
from the acetabulum (the articulation point of the femur with the pelvic girdle)
somewhat like three spokes from a hub, with the ilium directed upward, the
pubis downward and forward, and the ischium downward and toward the
rear. In extant birds, the ilium has been greatly broadened and lengthened in
an anteroposterior direction and firmly fused to the synsacrum. The ischium
and pubis have each evolved into long, thin bars which are parallel to the
vertebral column. Due to the orientation of these bones, the area ventral to the
pelvis is open to accommodate the centrally placed abdomen.
Modem birds do not possess a long tail with vertebrae, as was present in
members of Archaeopteryx and other non-avian archosaurs. Instead, there are
about five caudal vertebrae and a pygostyle formed by the fusion of the
remaining vertebrae. The pygostyle supports the tail feathers, which function
in balancing and steering the bird.
The hindlimbs also are greatly modified. The fibula is reduced to a small
sliver, and this change results in a considerable loss in the ability to rotate the
lower legs so they move in a rather limited fore-and-aft direction. In the area of
the ankle, several tarsal bones are fused to the end of the tibia, which is
recognized as the tibiotarsus. The remaining tarsals are joined to the three
fused metatarsal bones, and this structure is called the tarsometatarsus. The
tarsometatarsus, which is raised high above the ground, adds speed for
running, reduces the risk of dislocation, and simplifies leg construction. Toes
are also reduced in modern birds. In all birds, the fifth toe is absent, and
further reduction occurs in various clades.
The forearm also has been greatly modified through its evolution into a
wing. The humerus has been shortened and broadened resulting in increased
area for muscle attachment, and the ulna has been broadened and provides a
base for the attachment of flight feathers. Bones of the hand have been greatly
reduced such that there are only two carpals (radial, ulnare), three metacarpals
(carpometacarpus), and three digits (digits 2-4).
®s~~five morphological features from the above text, how are these
mo 1; lcatzons functzonally advantageous for flight?
ECOMORPHOLGY OF BIRDS
ir:
Birds (Aves) have invaded man t
s of h .
.
are often reflected in various aspect y
abltats, and their feeding habits
bird skins and/ or skeletons are ava ~l Obi e~ m~frphology, especially the beak. If
ecom
h'
..
1 a e, 1 entI y each of the following
orp s USIng the gIven descriptions. (Pough et al., 1999).
Sand Prober - This type of beak is extrem 1 1
.
long for wading Example
d'
e y ong and thIn; the legs are often
.
s are san pIpers and killdeer (Charadriiformes).
Fish Eater - This type of beak is relativ 1 1
.
often long. Examples includ h e y on.g an~ spear-lIke; the legs are
(Charad " f )
e erons, egrets (Clconnformes), terns
rn ormes, and cormorants (Pelecaniformes).
Raptor - The beak is short hooked and h
muscular. Examples includ~ owls (St' -/ arp-)edged; legs are stout and
rIglormes and hawks (Falconiformes).
Water Strainer - The beak i r e1 f 1
the edges for holding food :at ~ ~ve y
include ducks (Anseriformes)
s~ort, flat and broad, and has 'frills' on
a~~afl~:~~g~:r(~~~:~i;:::e~~t.Examples
Insect Eater - The beak is relativel 1
(f'
.
(rather like forceps). Examples inclJ"d ong b~r the SIze of the bird) and pointed
(Passeriformes).
. e war ers, wrens, and fly catchers
Seed Cracker - The beak is short stubb
d
sparrows, finches (Passeriformes) , d y, an sharp-edged. Examples include
,an parrots (PslttaClformes).
Insect Netter - The beak is very short flat
db
bristles (modified feathers) on 'th
'd' f' an road. There are sometimes
.
.
el er SI e 0 the beak f d t .
.
l ' or e ectmg or catchIng
Insects. These birds catch insects in flight E
(Caprimulgiformes), swifts, and
mghthawks
swallow~ (;::~r~~~:~~~e
l
Nectar Feeder - The beak is Ion and
and protrusible. Examples incl
h narrow: and the tongue is relatively long
u e ummmgb Irds (Apodiformes).
218
LABS FOR VERTEBRATE ZOOLOGY
Lab 7: AMNIOTA: REPTILIA
219
QUESTIONS FOR DISCUSSION
~AThY are there no viviparous birds? Turtles? Discuss this question in the
~(D'~o ntext of a phylogenetic perspective.
2.emperature-dependent sex determination (TDSD) is a complex trait that is a
synapomorphy for Reptilia. Note, however, that it is present in Chelonia,
Lepidosauria, Crocodylia but not Aves. Why might this be the case?
3. The dinosaur-bird hypothesis has received wide attention of late, and is
discussed in Pough et al. (1999), as well as many other sources. What are its
strengths? Its weaknesses?
4. One of the more recent influential papers on the utility of phylogenetic
systematics in comparative biology is by Schwenk (1994a). In this paper he
shows the failure of phenetic approaches (and paraphyletic classifications)
for accurately interpreting aspects of the sensory biology of squamates, the
taxon studied in this lab. As a class, discuss this paper and apply Schwenk's
views and conclusions to other areas of study of squamates, such as mating
systems and tongue morphology. [See other papers by Schwenk (1994b, 1995)
and by Cooper (1996)].
WEB SITES
There are multiple Web sites that you can explore, and again, it is prudent
that you visit the sites such as Tree of Life and others presented in Lab 1 for
information on reptilians. The one we provided below is an excellent start.
<http://www.flmnh.ufl.edu/natsci/herpetology/crocs.htm>.
This Web site is maintained by the Crocodile Specialist Group (CSG), a
worldwide network of professional and lay people, as well as a variety of
organizations that are concerned with and involved in the conservation of all
species (23 extant species) of crocodylians. The CSG has over 350 members and
operates under the auspices of the Species Survival Commission of the IUCN
(The World Conservation Union). This is an excellent Web site for up-to-date
information on crocodylians and profiles of all species. Also, there are many
links to other sites concerning crocodylians, including those on systematics.
Colbert, E.H., and M. Morales ]991 E I '
New York.
' . vo utwn of the Vertebrates. 4th edn. Wiley-L' N
~~~
onant, R, and I.T Collins. 1991. A Field Guid t
.
'
C
North America. Houghton Mifflin Bosto: ~Reptl~s and Amphibians of Eastern and Central
ooper, W.E., Jr. 1996. Variation and e;oh;tion'of :s:ac usetts. .
Herpetological Natural History 4: 135-150 0 ked tongues m squamate reptiles.
E
stes, R, and G. PregilL (Eds.). 1988. Ph 10 ene '.
.
.
Umversity Press, Stanford Califor~iag tIC Relatwnshlps of the Lizard Families. Stanford
C
.
Feduccla, A. 1996. The Origin and Evolution 'of B'
Connecticut
" lrds. Yale Umversity Press New H aven
•
Gauthiel~ I. 1986. Saurischian mono
I
h 1 a
'
..
'
nd th~.'.lflgm of birds. In The Origin of Birds and th
n ,pp. 1-:);). MemOIrs of the California Academ of e
E~olution of Flight (Ed. by K. pfdi~ ~
SCIences, No.8.
Gauthier, JAG
Y
."' . . . Kl
, uge, and T. Rowe. 1988 A
.
CladlslIcs 4: 105-209.
. mmote phylogeny and the importance of fo '1
G~ HW
'
=s.
ne, . .1997. Snakes. The Evolution of M st
.
K
Berkeley and Los Angeles California y ery In Nature. University of California Press
emp, TS. 1988
.' or Archosauria?
,.
'
. ' Haemoth ermra
Th .
'.
crocodIles. Zoological Journal of the I .
. Se mterrelatlOnshlps of mammals birds and
,.mnean oClety 92: 67-104.
"
Poe, S. 1996. Data set incon ruen
393-414.
g
ce and the phylogeny of crocodilians. Systematic Biology 45:
Pough, EH., R.M. Andrews '"
J E Cadle'M
" L C rumpAHS 'tk
Herpetology. Prentice-Hall U er S ddl . ' . . aVI z y, and K. D. Wells. 1998.
Pou 1 FH
.
,pp
a
e RIver, New Jersey.
g 1, . ., e.M. Jams, and I.B. Heiser. 1999 Vertebra L" . River, New Jersey.
.
te 1;e. ~th edn. Prentice-Hall, Upper Saddle
Pntchard, p. 1979. Encyclopedia oJIurtles TFH P
. .
Rleppe!, 0., and M. deBraga. 1996 Turties·a··' ubhcatlO~s, Neptune, New Jersey.
Romer, A. S., and TS. Parsons 198'6 T' " s drapsId reptIles. Nature 384: 453-455
.,
. rle vertebrate Body 3 d d
.
' r e n. Saunders College Publishing,
N ew Yark, New York.
Schultze, H-P., and 1,. Trueb. 1991 Ori ins of th e .
Consensus. Comstock PUblishing~s~o . t Hllghher Groups of Tetrapods: Controversy and
Schwenk,K. 19940, . Wh y sna k es have fa k dCIat es, t aca, New York .
Schwenk, K. 1994b Comparat'b' 1 r e ongues. S,cience 263: 1573-1577
.
,
,lve 10 ogy and the'
'.
study from the sensory biology of squ t ImPlPrtance of cladistic classification: a case
SOCIety 52: 69-82
rna e replI es. BIOlogical Journal of the LI'
Sh '
nnean
c wenk, K. 1995. Of tongues and noses' chemore
'"
. Ecology and Evolution 10: 7-12.'
ceplIon In lIzards and snakes. Trends in
Shme, R. 1988. Parental care in reptiles In Biolo a th
..
Gans and R Huey) pp 275-329'B'
B gy if e Reptlila , Vol. 16, Ecology B (Ed by C
.
. anta
.
Shi
199]
,ne, R'
. Australian,
Snakes.
A Natural
Histooks Ann A rb or, M'Ichlgan
(reprinted in" 1994)
Stebbms: Re. 1985. Field Guide toWestern Re til~:~'nd ~nell UnIversity Press, Ithaca, New York.
GUIde Series. Houghton Mifflin B t p
mphlblans. 2nd. edn. Peterson Field
Welty, I.e., and 1,. Baptista 1988 Th 'L' as on,assachusetts.
York, New York.
.
. e ife of BIrds. 4th edn. Saunders College Publishing, New
C
M
REFERENCES
Benton, M.J., and J. Clark. 1988. Archosaur phylogeny and the relationships of the Crocodylia.
In: The Phylogeny and Classification of the Tetrapods, VoL 1 (Ed. by M. J. Benton), pp. 295-338.
Systematics Association Special Volume 35A, Clarendon Press, London, England.
Cogger, H.G. 1994. Reptiles & Amphibians of Australia. Cornell University Press, Ithaca, New York.
220
LABS FOR VERTEBRATE ZOOLOGY
Lab 7: AMNIOTA: REPTILIA
221