Friday, January 31, 2014

Biology of the Reptilia
By: Megan Landon, Cameron Eddy, and Vince Ziccardi
Laboratory #2: Testudines

Key Points Covered in Lab:
1.       Turtle Anatomy of the skeleton
Sea turtle skull exhibiting anapsid
condition and keratinized beak.
2.       Reproduction of Turtles
3.       Turtle Diversity

Let’s Get a Quick Glimpse on Testudines!
·         There are 327 species of turtles categorized into 14 Families
·         Turtle distribution is everywhere worldwide except for Antarctica
·         Can live in habitats of marine, terrestrial, and freshwater
·         Special morphology of the carapace and plastron (will be discussed later)
·         Turtles lay eggs and are therefore oviparous
·         Mothers typically bury their eggs into a nest and never return to it!
·         Extant turtles lack teeth but have keratinized beak
·         Skull is anapsid (no temporal fenestra)
·        Testudines emerged in Triassic period (210-220 mya)

Extinct Ancestors of Modern Turtles:

1.       Proganochelys quenstedti: note that they possessed teeth, carapace, plastron, long tail with turtles and limbs held inside the ribcage

2.       Odontochelys semitestacea:  They possessed teeth, a plastron but no carapace! 

The Turtle Skeleton: Unlike most reptiles, the turtle skeleton is very unique due to its two parts: the carapace and plastron!

Carapace and Plastron Bones
a.       Carapace Bones
                                                               i.      Formed by fused ribs (costal bones) and vertebrae in trunk region (neural bones)
                                                             ii.      Note the outermost bones (peripheral bones), the base of the spine (sacral bone), the posterior end (pygal), the anterior end near the neck (nuchal bone), and the suprapygal bone which is between the sacral and pygal bones

Bones of the carapace: A) Nuchal B) Neural C) Costal D) Sacral E) Suprapygal F) Pygal G) Peripheral
b.      Plastron Bones
                                                               i.      Most anterior lateral pair of bones (epiplastron), posterior lateral pair of bones (xiphiplastron), the median plate on anterior side (entoplastron)
                                                             ii.      Note how the hyoplastron is above the hypoplastron with the mesoplastron in-between the two lateral pairs of bones

Bones of plastron: A) Epiplastron B) Entoplastron
C) Hyoplastron D) Hypoplastron E) Xiphiplastron

Carapace and Plastron Scutes
a.       Carapace Scutes
                                                               i.      Note that the vertebral scutes cover the spinal region, the pleural scutes cover the ribs, and the marginal are the outermost scutes
                                                             ii.      Also note how the supramarginal scutes fall in-between the marginal and pleural; the cervical scute covering the neck region of the turtle
Scutes of the carapace: A) Vertebral B) Pleural C) Marginal D) Cervical
Supramarginal scutes present on carapace of Macrochelys temminkii, but not Chelydra serpentina

b.      Plastron Scutes
                                                               i.      Note the intergular scutes covering the throat of the turtle (anterior) and the anal scutes (posterior); the gular scutes are first lateral pair followed by the humeral scutes which are underneath
                                                             ii.      The pectoral scutes are laterally paired near the pectoral girdle (note how the axillary scutes cover the pectoral girdle), the abdominal scutes cover the abdomen (inframarginal scutes are outside abdominal scutes), and the femoral scutes covering the femur of the turtle
Plastron scutes: A) Gular B) Humeral C) Pectoral D) Abdominal E) Femoral F) Anal G) Inframarinal H) Axillary

***A note on Carapace/Plastron Scutes vs. Carapace/Plastron Bones

(The scutes covering the bones and both the carapace and plastron do not directly align with each other.)

Girdles of Turtles
a.       Pectoral Girdle
                                                               i.      contains two parts of the scapula and a coracoid
Turtle pectoral girdle: A) Dorsal process of scapula
 B) Ventromedial process of scapula C) Coracoid

b.      Pelvic Girdle
                                                               i.      the ilium (sticking out in the back), the ischium (the two posterior bones on pelvic girdle), and the pubis (the two anteiror bones of the pelvic girdle)
Turtle Pelvic girdle: A) Ilium B) Pubis C) Ischium

Turtle girdles: A) Pectoral B) Pelvic
Here’s a different look by showing the entire skeleton of the turtle. Try to see if you can identify the bones associated with the pectoral and pelvic girdles.

      Turtle Skulls
a.       Note the prefrontal, frontal, parietal, and postorbital bones on the dorsal view of the turtle skull
b.     On the ventral view, note the premaxilla, maxilla, pterygoid, palatine, vomer (separating the right and left nasal cavities), supraoccipital, basioccipital and exoccipital
c.       On the lateral view of the turtle, note the jugal, quadratojugal, quadrate

Dorsal, ventral, and lateral view Chelydra seprentina  skull. A) Supraoccipital B) Squamosal C) Exoccipital D) Parietal E) Postorbital F) Frontal G) Prefrontal H) Maxilla I) Premaxilla J) Jugal K) Quadratojugal L) Quadrate M) Pterygoid N) Basioccipital O) Vomer P) Palatine

Both sexes of turtle have anatomical characteristics, unique from both each other and from other reptiles, that allow scientists to differentiate between sexes as well as aid in the act of reproduction. In determining the sex of the turtle, the easiest way is to look at the tails.  Males have a larger, fatter, overall more robust tail than females who have shorter less robust tails.
Comparing the tail sizes of female (left) and male (right) turtles
When these tails are laid straight, the cloaca of the male turtle can be found well beyond the posterior margin of the carrapace whereas the cloaca of the female is found before/ as the posterior margin of the carrapace(Fig. X).
 Ventral view of the male plastron and female plastron
Posterior view of the male  (right) and female (left) plastron
The unique reproductive characteristics of turtles are found mainly in males. Males have a concave plastron to keep them from sliding off the female during copulation, they have longer forelimb claws which are used during courtship to "tickle" the face of the female

 Images comparing forearm claws (left) and cloaca position (right) of both male and female turtles

 and they have a intromittent organ, a large appendage similar to a penis that functions to transfer sperm.
Copulatory organ in male turtles

Turtles are typical amniotes and oviparous wherein they have internal fertilization resulting in a cleidoic egg laid outside the body. These cleidoic eggs have hard calcium carbonate shells to protect the embryo inside from the outer environment while also allowing gas exchange. The embryos inside the egg have direct development, meaning that when the babies hatch, they will be minature versions of their parents. (Check last week's lab for images)


About 200 to 250 million years ago, the order Testudines split between two groups: Cryptodira and Pleurodira. Turtles that belong to Cryptodira are more commonly known as "hidden neck turtles" meaning they pull their heads straight back into their shells when frightened.
Turtles that belong to Pleurodira are more commonly known as "side-neck turtles", so when they are frightened they pull their head to the side under the edge of their shells.

Ohio Diversity

Out of the multiple families and species of turtle that are found worldwide, Ohio is home to only 4 families and 12 species.
   Chelydridae - Chelydra serpentina (Common Snapping Turtle)
Macrochelys temminkii (top) and Chelydra serpentina (bottom)
  Kinosternidae - Sternotherus odoratus (Stinkpot Turtle)

   Trionychidae -
Apalone spinifera (Spiny Softshell Turtle)

                          Apalone mutica (Smooth Softshell Turtle)

   Emydidae - Chrysemys picta marginata (Midland Painted Turtle)

                     Clemmys guttata (Spotted Turtle)

                     Emydoidea blandingii (Blanding's Turtle)

                     Graptemys geographica (Map Turtle)

                     Graptemys pseudogeographica (False Map Turtle)

                    Pseudemys concinna (Hieroglyphica River Cooter)

                    Terrapene carolina (Eastern Box Turtle)

                   Trachemys scripta (Red-Eared Slider)

Lab #2: Testudines (Nick Spies and Alex Murray)

Lab #2: Testudines
There are currently 327 identified extant species of Testudines, placed into 14 families.  In this specific lab, 8 of these extant Testudines families were examined and described.  The eight specific Testudine families that were examined in this lab are as follows:
  1. Podocnemidae (Madagascan Big-Headed Turtles & American Side-Neck Turtles)
  2. Chelidae (Australoamerican Side-Neck Turtles)
  3. Trionychidae (Soft-Shell Turtles)
  4. Cheloniidae (Hard-shelled Seaturtles)
  5. Chelydridae (Snapping Turtles)
  6. Kinosternidae (Mud and Musk Turtles)
  7. Testudinidae (Tortoises)
  8. Emydidae (Cooters, Sliders, American Box Turtles)
Figure 1: Phylogenetic Relationships of Turtle Families 
Pleurodira and Cryptodira Testudines 
Within the Testudines, there is a basil split between Pleurodira and Cryptodira.  The two following terms refer to how Testudines hide their heads when they are frightened.  Pleurodiran turtles fold their head either to the right or to the left, and cannot pull their heads into their shells (Fig. 1)(Fig. 2).  Cryptodiran turtles pull their heads into their shells within a pocket, during this process, the turtle's neck curves posteriorly in an "S" shape(Fig. 1)(Fig. 2).

Figure 2: Pleurodira vs. Cryptodira Neck Retraction
Two Pleurodira Testudine Families Examined in Lab:

1) Podocnemidae (Madagascan Big-Headed Turtles & American Side-Neck Turtles)

Location: South America & Madagascar 
3 Genera, 8 Species 
Moderately Large
River Turtles
Broad, domed, streamlined shells
Active Swimmers
Herbivores/Opportunistic carnivores
Nest in sand along river 
 2) Chelidae (Australoamerican Side-Neck Turtles) 

Location: South America, Australia, Indonesia 
(Southern Hemisphere only) 
Flattened Skull and Shell
Primarily Aquatic
Some leave water to forage during rains near water
(Gulp Feeding)                                

Six Cryptodira Testudine Families Examined in Lab:

1)Trionychidae (Soft-Shell Turtles)

 Location: Africa, Asia, New Guinea, SE Asia, Indonesia, North America

Snorkel-like snout
Flattened "Pancake"
Reduced Carapace/Plastron
Lack epidermal scutes
Possess thick, leathery skin
Long Necks
Some Possess femoral flaps on plastron

Lattice-like plastron, either fused or separate, hyoplastron and hypoplastron 
Opportunistic carnivores 
Cutaneous Respiration (from not having scales)

2)Cheloniidae (Hard-shelled Seaturtles)
Location: Tropical to Subtropical Oceans
Flat streamlined shells with epidermal scutes 
Forelimbs flipper like
Hind limbs webbed for steering 
Emerge on beaches only to nest 
Require 25 years for sexual maturity 

3)Chelydridae (Snapping Turtles)
 Location: Eastern North America, Mexico & Central America, Northern South America
2 Genera, 2-5 Species
Large Heads (relative to body)
Skull roof deeply emarginated
Broad, flat Carapace
Reduced Plastron (cruciform)
Longest tail of any Testudine
Aquatic, only on lad to lay eggs
Opportunistic carnivores
Primarily Herbivores

**Two genera of Chelydridae are Chelydra (common snapping turtles) and Macrochelys Alligator Snapping Turtle**

  • Biggest difference between the two species is that Macrochelys has four marginal scutes, whereas Chelydra

4)Kinosternidae (Mud and Musk Turtles)
Location: North America, Central America, and Northern South America (New World Only)
24 + species 
Smallest Testudines
Oblong, moderately domed carapace
Large heads compared to body size
Plastron commonly hinged
Reduced plastron 
<10 epidermal marginal scutes 
Entoplastron sometimes present
Generally aquatic
Bottom walkers 
Hibernate on land 
Can forage on land 
Occupy underground retreats/nest communally 
Occasionally nest below vegetation  

5)Testudinidae (Tortoises)

Location: North/South America, Galapagos, Africa, Madagascar, Seychelles, Europe, Asia, Indonesia 
15 Genera, 45+ Species
Almost all have domed shells 
Columnar/Elephantine feet
Terrestrial (Desert, Grassland, Scrub)
100 days incubation to 18 months

6)Emydidae (Cooters, Sliders, American Box Turtles)

    **two Testudine subfamilies within this Testudine family, Emydinae (Fig. 3) and Deirochelinae (Fig. 4)

Figure 3: Subfamily: Emydinae, Genus: Clemmys

Figure 4: Subfamily: Deirochelinae Genus: Graptemys
Location: North America, Central America, Parts of South America, Europe, Asia, North Africa
42 species
Medium Sized Turtles
Plastron large, occasionally hinged
Sexual Dimorphism common (females 2X larger than males)
Omnivores or strongly herbivorous 

Two Subfamilies:
1) Emydinae: conservative diets, diversity of habitats, some plastrons hinged 
2) Deirochelinae: Diversity of diets, conservative habitats, aquatic, diet specialists, epipubes do not ossify 

Testudine Anatomy
Skeletons of Testudines are the most unique skeletons of any other type of reptile, because of the presence of a sell structure.  The shell structure is formed by two main skeletal structures, the carapace and the plastron.  The carapace (Fig. 5 & 6) is formed of broadly expanded and fused ribs and vertebrae in the trunk region, as well as a layer of dermal bones that span the spaces between these bones.  The plastron (Fig. 5 & 6) is composed of several paired bones that are remnants of the sternal elements and perhaps the gastralia.  Positioned within the shell structure are the pectoral girdle and forelimb, and the pelvic girdle and hind limb. 
           Bones of the Carapace: (Fig. 5 & 6)                                     Bones of the Plastron: (Fig. 5 & 6)
           Nuchal                                                                                     Epiplastron
           Peripheral                                                                                Endoplastron
          Neural                                                                                      Hyoplastron
          Costal                                                                                      Mesoplastron
          Suprapygal                                                                              Hypoplastron
          Pygal                                                                                       Xiphilplastron 

Figure 5: Bones of Carapace and Plastron 

Figure 6: Bones of Carapace and Plastron examined in Lab 2: Testudines 

Overlaying the bony skeleton of Testudines is a thin layer of epidermis.  This epidermis produced large plate-like scale, referred to as scutes (Fig. 7 & 8).  

Scutes of the Carapace (Fig. 7 & 8):                                 Scutes of the Plastron (Fig. 7 & 8):

Cervical                                                                                Intergular 
Marginal                                                                              Gular  
Supramarginal                                                                     Axillary 
Vertebral                                                                             Humeral
Pleural                                                                                 Pectoral 

Figure 7: Scutes of the Carapace and Plastron 

Figure 8: Scutes of the Carapace and Plastron examined in Lab 2: Testudine

Girdle of Testudine 

Figure 9: Pelvic Girdle of Testudine 
Figure 10: Pectoral Girdle of Testudine 

                                   Testudine Skull

Testudines have the skull condition known as an Anapsid skull (Fig. 11 &12).  Although Testudines demonstrate the Anapsid skull condition, many Testudine species have a deep temporal emargination on the posterior margin of the skull. 

Figure 11: Anatomy of Testudine Skulls examined in Lab 2: Testudines

Figure 12: Skull Anatomy of Testudine

Exhibit internal fertilization
Direct Development of embryos inside a cleidoic egg
Shell is hard or pliable and composed of calcium carbonate shell units
All are Oviparous

1.Typically have a concave or slightly concave plastron to prevent them from sliding off females (Fig. 13)
2. Males typically have longer forelimb claws (Fig. 14)
3. Males have a very large copulatory organ, the intromittent organ, its purpose is like a penis to transfer sperm (Fig. 15)

A good way to tell difference between male and female Testudines is by examining the tail. Males tales will be fatter and more robust than the females, and when the tail is gently straightened, the cloaca will be exposed, clearly behind the posterior edge of the carapace, while the female cloaca is positioned at or before the posterior edge of the carapace (Fig. 16).
Figure 13: Comparison of Male Testudine and Female Testudine Carapaces
Figure 14: Presence of Longer Forelimbs on Male Testudines 

Figure 15: Presence of Intromittent Organ in Testudines
Figure 16: Male Chelydra (Visual of Cloaca Posterior to Carapace)
The Arrow here point to the exposed cloaca, based off the position, this is a male Chelydra (common snapping turtle)

Ohio Diversity of Testudines 

Chelydridae (Snapping Turtles):
Chelydra serpentina (Common Snapping Turtle) 

Kinosternidae (Mud & Musk Turtles):
Sternotherus odoratus (Stinkpot Turtle)
Trionychidae (Soft-Shell Turtles):
Apalone spinifera (Spiny Softshell Turtle)
Apalone mutica (Smooth Softshell Turtle)
Emydidae (Cooters, Sliders, American Box Turtles & Allies):
Chrysemys picta marginata (Midland Painted Turtle)
Clemmys guttata (Spotted Turtle)

Emydoidea blandingii (Blanding’s Turtle)
Graptemys geographica (Map Turtle)
Graptemys pseudogeographica (False Map Turtle)
Pseudemys concinna (Hieroglyphica River Cooter)
Terrapene carolina (Eastern Box Turtle)
Trachemys scripta (Red-Eared Slider)