Friday, March 23, 2012

Lab #6 Serpentes and Ophidia: Alex Valigosky and Jeff Walker

Serpentes and Ophidia

Serpentes, or the snakes, are Lepidosaurs, and more precisely Squamates.  This puts them in the clade that contains all of the lizards; snakes are highly-derived lizards.  A major united characteristic of snakes is the evolutionary loss of legs, though, as we have pointed out in the previous blog about lizards, leglessness has evolved multiple times and Serpentes are not the only legless lizards.  Artifacts of legs and pelvic girdles can be spotted in basal snakes, such as members of Boidae, as small projections called spurs near the cloaca that aid the snakes in mating.

The tree of life - Serpentes
The tree above details the hypothesized evolutionary relationships of various clades of Serpentes.  The most basal members are those of the Scolecophidia (worm snakes, blind snakes, and file snakes); these are mostly tiny fossorial snakes that live under ground or in the substrate.  The Alethinophida are the "real snakes".  This clade includes the Henophida (old snakes) and Caenophida (new snakes).  It is within the Henophida that we find such families as the Pythonidae and the Boidae and within the Caenophidia that we find families such as the Colubridae, the Viperidae, and the Elapidae. While there may be as few as 16 families, most of which are certianly monophyletic, depending upon the possible elevation of various subfamilies to family status, there may very well be many more.  

Lily - Ball Python - Python regius
Pythonidae, the pythons, is a clade of 8 genera and some 37 species, found throughout sub-saharan Africa and through south and south east Asia and Australia.  These large constrictors can live in various habitats and are all oviperous (clutch increases proportional with body size). Pythons have the incredible adaptation of cranial infrared receptors located in interlabial pits, which allow them to see heat (these evolved independently of the infrared receptors of Viperidae, below).    

Boidae, the Boas (2 subfamilies with 11 genera, and over 60 species), can be found in western North America to southern sub-tropical South America, the West Indies, central Africa to south Asia, Madagascar, and in the South-west Pacific Island.  These are also small to large constrictors; they also have cranial infrared receptors located in interlabial pits and cloacal spurs.

Colubridae is an extensive and diverse, but certainly monophyletic group of snakes.  Seven sub-families are recognized, including: Colubrinae, Natricinae and Dipsadinae. This is a highly specious group with a world-wide distribution.

The Colubrinae is a grab-bag of misfit colubrids.  8 genera can be found in Ohio: Opheodrys vernalis (smooth green snake), Opheodrys aestivus (rough green snake), Coluber constrictor foxii (blue racer, above center), Coluber constrictor constrictor (northern black racer), Pantherophis obsoletus obsoletus (black rat snake), Pantherophis vulpina (fox snake, above upper-right), Lampropeltis triangulum triangulum (eastern milk snake, above left), and Lampropeltis getula nigra (black kingsnake; Lampropeltis getula californiae, california kingsnake pictured above lower-right, *not an Ohio species, but closely related)

The Natricinae mainly prey upon fish and amphibia (1 species known to eat crayfish, the queensnake). They are generally freshwater snakes and semi-aquatic or fully aquatic, and found throughout North America to northern Central America, Africa and Eurasia.  American species are exclusively viviparous, whereas old-world taxa tend to be oviperous.  There are some 13 species found in Ohio: 5 species of Thamnophis (garter snakes, above top-left (2 snakes), bottom-left, and ribbon snakes), 3 species Nerodia (water snakes, above top-center, bottom-center), 3 species of Storeria (Brown and redbelly snakes), Regina septemvittata (queen snake, above bottom-right and top-right), and Virginia valeriae valeriae (eastern smooth earth snake). 

 The Dipsadinae [Also known as the Xenodontinae] can be found throughout the new world.  These are diurnal hunters (with long muscular bodies and slender heads) or nocturnal hunters/searchers (with slender bodies and blunt, over-sized heads).  Clutch size is highly variable (directly associated with body size).  Four species can be found in Ohio: Diadophis punctatus edwardsi (northern ringneck snake), Heterodon platyrhinos (eastern hognose snake, above left and bottom-right), Carphophis amoenus amoenus (eastern worm snake, above center and upper-right), and Carphophis amoenus helenae (midwest worm snake).

Viperidae, the vipers, includes 3 subfamilies: Azemiopionae, Crotalinae, and Viperinae, with a total of 40 genera.  Vipers have a world-wide distribution with the exception of Papuaustrailia and the oceanic islands. These are highly venomous snakes with highly derived fang-apparati (solenogyphous fangs, the maxilla is highly kinetic).  Many vipers have cranial infrared receptors in loreal pits or beneath scale surface (as opposed to the  interlabial pits of old-snakes) and many of the more-derived species also have rattles.  There are 3 Ohio species (pictures to be added soon - camera malfunction): Agkistrodon contortrix mokasan (northern copperhead: mokasan),  Sistrurus catenatus catenatus (eastern massassauga), and Crotalus horridus (timber rattlesnake).  The massassauga rattlesnake is wet/prairie specialist, while timber rattlesnake is hardwood-forest specialist; copperheads lack rattles.

Elapidae (pictures to be added soon - camera malfunction) - (southern North America to southern South America, Africa, southern Asia to southeastern Australia, and the tropical Indian and Pacific oceans) some of the most highly venomous snakes and includes many marine taxa.  There are two sub-families: Elapinae includes the cobras, mombas, crates, and the Hydrophiinae, which includes the sea snakes (recognizable by their reduced ventral scales and laterally flattened caudal regions; adaptations obtained in the move from land to back to water).  Elapinaes are primarily terrestrial, some are arboreal and fossorial.

Lab 6: Serpentes & Ophidia (Dan Paluh and Sean Harrington)

In this lab we continued looking at members of Squamata, the clade that includes lizards and snakes, focusing specifically on snakes (Serpentes/Ophidia) this time. Squamates are members of Lepidosauria, which also includes Sphenodontida, and the general characteristics of these clades are described in our “Lepidosauria part I” blog. As was also discussed in the earlier blog, snakes are highly derived lizards, such that the clade Sauria, which traditionally included only lizards, should be expanded to include snakes and lizards to make it monophyletic. Snakes are limbless (although some retain rudiments of the hind limb and pelvic girdle), lack external ear openings, and lack eyelids. The elongation of snakes is primarily achieved by elongation of the trunk and increases in the number of presacral vertebtrae.

Due to their lack of limbs, most snakes must consume their prey whole (those that don’t dismember their prey with their coils and then swallow the pieces whole), and derived snakes have highly specialized and kinetic skulls that allow them to swallow prey that may be much larger than a snake’s own head. Snake exhibit extreme streptostyly, meaning that the quadrate articulates loosely with the supratemporal at its dorsal end and the lower jaw and its ventral end, which makes the lower jaw highly mobile. Snakes also have kinetic articulations between the supratemporal and parietal, dentary and compound bone of the lower jaw, prefrontal and maxilla, and frontal and maxilla. Snakes also have a ligamentous mandibular symphysis between their dentaries, which allows the right and left sides of the jaws to stretch apart, further facilitating the swallowing of large prey. Points of articulation are circled in the figure below.

Most snake teeth are recurved, conical, or laterally compressed, and are solid and lack grooves. These teeth are referred to as aglyphous and are the only type of teeth present in Clades such as Boidae and Pythonidae. Many snakes possess specialized enlarged teeth that aid in venom delivery (fangs) in addition to the relatively unspecialized aglyphous teeth. Fangs fall into three categories: 1) opisthoglyphous fangs are found in members of Colubridae, and are enlarged teeth at the posterior end of the maxilla which may or may not be grooved to aid in venom delivery; 2) proteroglyphous fangs are found in members of Elapidae, and are enlarged, hollow teeth used for venom delivery and positioned on reduced, immobile or relatively immobile maxillae at the front of the mouth; and 3) solenoglyphous fangs are found in members of Viperidae, and are enlarged, hollow teeth used for venom delivery that are positioned at the front of the mouth on reduced, highly mobile maxillae, which allow the fangs to swing outwards during a strike.

(Vonk et al., 2008)

Serpentes Diversity

Family Pythonidae (8 genera, 37 species): Pythons are found in Sub-Saharan Africa and South and Aoutheast Asia to Australia. They occur in a variety of habitat, from rain forests to deserts to semiaquatic environments. Cranial infrared receptors in interlabial pits are found in many species of pythons. All members of Pythonidae have aglyphous teeth, with no specialized fangs. All pythons are oviparous and some species possess remnants of limb or girdle elements.

Family Boidae (2 subfamilies): Boas are found in Western North America to southern South America, West Indies, central Africa to South Asia, Madagascar, and Southwest Pacific Islands. Cranial infrared receptors in interlabial pits are found in many species of boas. All members of Boidae have aglyphous teeth, with no specialized fangs. Hindlimb vestiges are present as cloacal spurs and pelvic remnants remain in some species of Boidae.

Subfamily Boinae (7 genera, 47 species): Members of Boinae are characterized by having labial sensory pits and caudal vertebrae that have simple neural arches. All members are also viviparous. Many members are arboreal, although the species Eunectes is aquatic.

Subfamily Erycinae (4 genera, 17 species): Members of Erycinae are characterized by lacking labial sensory pits and caudal vertebrae that have forked neural arches. Some members of this subfamily are semifossorial, and occur in arid to moist habbits. All members are also viviparous.

Family Colubridae (7 subfamilies): Colubridae is the most speciose family of snakes, and taxonomy within this clade is still being resolved. Colubrids possess either opisthoglyphous or completely aglyphous dentition, lack infrared receptors, and possess no remnants of limb or girdle elements. They are found worldwide, except for on Antarctica and oceanic islands, and inhabit a wide range of habitats.

Subfamily Colubrinae (100+ genera, ± 650 species): Colubrinae is a highly diverse subfamily with a worldwide distribution and few defining characteristics. Colubrines exhibit a wide range of body forms, and range from aquatic to desert inhabitants to inhabitants of montane forests. They range from fossorial to arboreal, and may be dietary specialists or generalists. Colubrines are primarily oviparous, though some taxa are viviparous. Colubrinae contains several Ohio species: 1) Opheodrys veralis (smooth green snake), 2) O. aestivus (rough green snake; observed in lab), 3) Coluber constrictor foxii (blue racer; observed in lab) and C. c. constrictor (northern black racer), 4) Pantherophis obsoletus obsoletus (black rat snake; observed in lab), 5) P. vulpinus (fox snake; observed in lab), 6) Lampropeltis triangulum triangulum (eastern milk snake; observed in lab), and 7) L. getula nigra (black kingsnake; observed in lab). Colubrinae also includes the indigo snake, Drymarchon corais, which is the largest North American snake.

Subfamily Dipsadinae (90+ genera, 700+ species, synonym: Xenodontinae): Dipsadinae is another highly diverse subfamily of colubrids. Dipsadines are found in the Americas and inhabit all non-marine habitats. They range from terrestrial to arboreal, and most are dietary generalists. Members of Dipsadinae are opisthoglyphous. Dipsadines are primarily oviparous. Dipsadinae includes several Ohio species: 1) Diadophis punctatus edwardsi (northern ringneck snake; observed in lab), 2) Heterodon platyrhinos (eastern hognose snake; observed in lab), and 3) Carpophis amoenus (worm snake; observed in lab).

Subfamily Natricinae (38 genera, 195+ species): Many natricines are semiaquatic to aquatic in freshwater, with others being primarily terrestrial to semifossorial. Aquatic species prey primarily on fish and amphibians, though some are dietary specialists. All New World natricines are viviparous, and Old World natricines are primarily oviparous. Members of Natricinae are opisthoglyphous. Natricinae contains several Ohio species: 1) Nerodia sipedon sipedon (northern water snake; observed in lab), N. s. pleuralis (midland water snake); 2) Nerodia erythrogaster neglecta (copperbelly water snake); 3) Regina septemvittata (queen snake; observed in lab); 4) Thamnophis butleri (Butler’s garter snake); 5) T. sirtalis sirtalis (eastern garter snake; observed in lab); 6) T. radix radix (eastern plains garter snake); 7) T. sauritus sauritus (eastern ribbon snake); 8) T. s. septentrionalis (northern ribbon snake); 9) Storeria dekayi (brown snake; observed in lab); 10) S. occipitomaculata occipitomaculata (northern redbelly snake; observed in lab); and 11) Virginia valeriae valeriae (eastern smooth earth snake).

Family Elapidae (2 subfamilies): Elapids are found from Southern North America to southern South America, Africa, southern Asia to southern Australia, and the tropical Indian and Pacific Oceans. All elapids are venomous and have proteroglyphous fangs. No cranial infrared receptors are present and girdle and limb elements are absent.

Subfamily “Elapinae” (17 genera, 130+ species): This somewhat diverse subfamiliy contains mostly terrestrial snakes, although some arboreal and aquatic species are present. They are mainly predators of vertebrates, and are mostly oviparous, although a few species are viviparous.

Subfamily Hydrophiinae (43 genera, 165+ species): This group of Elapids are characterized by having palatine bones that lack choanal processes. Both terrestrial and aquatic species are found within this subfamily. “True” sea snakes belong to this group, and are characterized by having a laterally compressed body, a paddle like tail, and loss of enlarged ventral scales. All sea snakes are viviparous. Sea kraits have good terrestrial locomotion, and are oviparous.

Family Viperidae (3 subfamilies): Viperidae has a very large distribution, and is considered worldwide except Papuaustralia and oceanic islands. All viperids are venomous and have solenoglyphous fangs. Cranial infrared receptors are present in some species and girdle and limb elements are absent externally and internally.

Subfamily Azemiopinae (monotypice, Azemiops feae): This species is found in southern China, Burma, and Vietnam. They lack labial pits and has a distinct choanal process of the palatine. Azemiopinae are semifossorial and it is unknown if they are oviparious or viviparous.

Subfamily Crotalinae (26 genera, 160+ species): Members of Crotalinae are found in Southwest and southern Asia and the Americas. They have loreal pit infrared receptors and have a small choanal process on the palatine. These snakes are mainly nocturnal, and prey mainly on vertebrates. They are found in a variety of habits, such as deserts, to cool mountain forests, to wet tropical lowlands. They are maninly terrestrial, but some species are semiaquatic and arboreal. Most are viviparous, although a small number of species are oviparous. Crotalinae contains several Ohio species: 1) Agkistrodon contortrix mokasan (northern copperhead, observed in lab); Sistrurus catenatus catenatus (eastern massassauga, observed in lab); and Crotalus horridus (timber rattlesnake, observed in lab).

Subfamily Viperinae (13 genera, 65+ species): Members of Viperinae are found in Africa, Europe, and Asia. They are characterized by lacking loreal pits and a choanal process on the palatine. Most members of this subfamily are terrestrial, and occur in desert to forest habitat. Many species are diurnal, although others are nocturnal hunters. This subfamily includes some species that are viviparous, and some that are oviparous.

Lab #6 Lepidosauria: Serpentes & Ophidia - Chris K & Cait F

SNAKES.  Of extant Eureptilia, as mentioned in the last lab, the sister to Archosauromorphs are Lepidosauromorphs. Squamata (lizards and snakes) belong to the latter. We've already explored the lizards in this group, but now it's time to talk about the snakes!

Snakes have a lot of distinguishing features from lizards; since leglessness has evolved in both lizards and snakes we look at skulls and fangs.

Snake skulls articulate on the quadrate bone involving the lower jaw, making it Streptostyly. You can see the snake below actively using this jaw opening feature to ingest prey larger than it's skull:They also can have re-curved, evolved teeth for securing food. Some species of snakes have fangs, which have evolved independently multiple times as teeth specialized to deliver venom to prey. The major teeth and fangs are:
  • Aglypous (no grooves, typical re-curved teeth found in all species of snakes)
  • Opisthogypous (rear-fanged - positioned on the back of the maxilla - with a conspicuous groove for delivering venom)
  • Proteroglypous (front-fanged, - positioned at the front of the mouth or reduced maxilla, typically static orientation, folded and hollow in the center)
  • Solenoglyphous (most-derived retractable teeth, hollow and pipe-grooved for deep venom injection - positioned on high maxilla)
Snake teeth and fangs:

Just like lizards, snake phylogeny is controversial and many hypothesizes have been proposed from morphological and behavioral data, but we work from the vantage point that 16 families have been determined. Here we looked at five families in particular.

1. Colubridae = Colubrids
: 7 subfamilies
  • Distribution: Worldwide except for Antarctica and oceanic islands
  • Characteristics: Colubrids are the most diverse paraphyletic family of snakes that includes aglyphous, opisthoglyphous and proteroglyphous taxa. Girdle and limb elements are absent externally and internally. They also lack infrared receptors.
*Ohio subfamilies:
: More than 100 genera
Distribution: Worldwide

Characteristics: Highly diverse biology and ecology, generalists and mostly oviparous.
Opheodrys vernalis (Smooth Green Snake): much of state

Opheodrys aestivus (Rough Green Snake): southern third of state

Coluber constrictor foxii (Blue Racer)

Coluber constrictor constrictor (Northern Black Racer)

Pantherophis obsoletus obsoletus (Black Rat Snake)

Pantherophis vulpina (Fox Snake)

Lampropeltis triangulum triangulum (Eastern Milk Snake)

Lampropeltis getula nigra (Black Kingsnake): southern part of state

>>Natricinae: 38 genera
Distribution: North America to northern Central America, Africa and Eurasia through the West Indies. Characteristics: Generally small and most are labeled aquatic snakes that specialize feeding on fish and amphibians (only leaving water for basking and reproduction)
Nerodia sipedon sipedon (Northern Water Snake)

Nerodia sipedon pleuralis (Midland Water Snake)

Nerodia erythrogaster neglecta (Copperbelly Water Snake)

Regina septemvittata (Queen Snake)

Thamnophis butleri (Butler’s Garter Snake)

Thamnophis sirtalis sirtalis (Eastern Garter Snake)

Thamnophis radix radix (Eastern Plains Garter Snake)

Thamnophis sauritus sauritus (Eastern Ribbon Snake)

Thamnophis sauritus septentrionalis (Northern Ribbon Snake)

Storeria dekayi wrightorum (Midland Brown Snake)

Storeria dekayi dekayi (Northern Brown Snake)

Storeria occipitomaculata occipitomaculata (Northern Redbelly Snake)

Virginia valeriae valeriae (Eastern Smooth Earth Snake)

>>Dipsadinae: over 90 genera
Distribution: Americas
Characteristics: Occur in all habitats except marine and are mostly generalist predators. These new world terrestrial snakes are also predominantly oviparous. They're also venomous but not powerful enough to do much damage to a human other than swelling.
Diadophis punctatus edwardsi (Northern Ringneck Snake)

Heterodon platyrhinos (Eastern Hognose Snake)

Carphophis amoenus amoenus (Eastern Worm Snake)

Carphophis amoenus helenae (Midwest Worm Snake)

2. Elapidae = Cobras, Kraits, Sea Snakes, Death Adders, Allies
: 2 subfamilies (Elapinae:17 terrestrial genera, Hydrophiinae:43 aquatic genera)
  • Distribution: Southern North America to southern South America, Africa, southern Asia to southern Australia and the tropical Indian and Pacific Oceans.
  • Characteristics: Elapids are venomous snakes that have and erect fang anteriorly on each maxillary bone, exemplifying proteroglypous dentation. Elapids lack infrared receptors in pits or surface indentations. The girdle and limb elements are absent externally and internally. The Elapinae are oviparous and semifossorial genera, while the Hydrophiinae are mostly aquatic with a characteristic "paddle tail".

3. Viperidae = Vipers: 3 subfamilies (Azemiopinae:1 genera, Crotalinae:26 genera, Viperinae:13 genera).
  • Distribution: Worldwide, except Papuaustralia and oceanic islands.
  • Characteristics: Viperids are venomous snakes. They have cranial infrared receptors that occur in loreal pits in crotalines or beneath scale surfaces. Most are viviparous although some lay eggs in clutches of ten. Subfamily Viperinae lack loreal pits. Girdle and limb elements are absent externally and internally. They have distinctly triangular heads and characteristic rotating solenoglypous fangs.
*Ohio Subfamily: Crotaline
(From left to right) Sistrurus catenatus catenatus (Eastern Massassauga) = Rattle, wet prairie specialists, Agkistrodon contortrix mokasan (Northern Copperhead: Mokasan) = No rattle, basal group, and Crotalus horridus (Timber Rattlesnake) = Rattle, hardwood specialists, dark tail

4. Boidae = Boas: 2 subfamilies

:7 genera
Distribution: The subfamily Booinea is found in tropical Americas (new world)
Characteristics: They are non-venomous constrictors with a stretostyly, most have infrared labial pits and vestigal pelvic elements, and they don't have fangs. They do have spurs which are small on arboral taxa and larger on terrestrial/aquatic taxa.
-Erycinae:4 genera
Distribution: The subfamily Erycinae is found in Africa, SE Asia, and Australia (old world).
Charcteristics: They lack labial pits altogether and are semi-fossorial snakes. They are viviparous with robust cylindrical bodies, small eyes, blunt heads, and short tails. They live in arid habitats so they are mostly nocturnal.

5. Pythonidae = Pythons: Only 8 genera (Aspidites, Antaresia, Apodora, Bothrochilus, Leiopython, Liasis, Morelia, Python)
  • Distribution: Sub-Saharan Africa, Southern and SE Asia and Australia.
  • Characteristics: They are large to giant in size and have longitudinally-oriented maxillaries and solid teeth. They have cranial infrared receptors in interlabial pits and forage above ground but some are semi-aquatic. Cloacal spurs are on hind limb vestiges of pelvic remnants and they are oviparous tending to coil around their eggs for incubation.