Amphibian Characteristics, Taxonomy, and Evolution

Matthew J. Gray, Ph.D. College of Agricultural Sciences and Natural Resources University of Tennessee-Knoxville

Goal of the Lecture

To familiarize students with characteristics of the Class Amphibia, the diversity of extant amphibians, and the fossil record of amphibians.

Reading Assignments:

1) Handouts.

2) Duellman and Trueb: pp. 424-443

Lecture Structure

I. Class Amphibia Characteristics

II. Extant Amphibia Families

III. Amphibian Fossil Record

1 What are Amphibians?

Ectothermic tetrapods that have a biphasic life cycle consisting of anamniotic eggs (often aquatic) and a terrestrial adult stage.

Kingdom: Animalia Phylum: Chordata Subphylum: Vertebrata Class: Amphibia (amphibios: “double life”) Subclass: Lissamphibia Orders: •Anura (frogs) •Caudata (salamanders) •Gymnophiona (caecilians)

Amphibia Characteristics

1) Cutaneous Respiration

•Oxygen and CO2 Transfer (moist) •Family Plethodontidae (lungless salamanders) •Gills (larvae, few adult salamanders), 2 Lungs (adults) Plethodon dorsalis 2) Two Types of Skin Glands •Mucous Glands (cutaneous respiration) •Glanular Glands (toxic secretions) ¾Paratoid Glands 3) Sensory Papillae in Inner Ear and Doubled Transmission Channels in Middle Ear •Colemulla-basilar Papilla •Opercular-amphibian Papilla (<1000 Hz) 4) Green Rods in Retina (excluding caecilians) •Function Unknown •Other Light Receptors: red rods, single and double cones 5) Bicuspid Pedicellate Teeth •Crown (above gum), Pedicel (connected to jawbone) •New Crown Emerges from Pedicel

Modern Orders of Amphibia

•Gymnophiona (caecilians) 9% 3% ƒ 167 species Caudates Caecilians

88% Anurans

Ichthyophis kohtaoensis 280 Species in U.S. (86 Species in TN) •Caudata (salamanders)

•Anura (frogs) Dendrobates tinctorius ƒ 5,420 species

Plethodon shermani ƒ 559 species

2 Caecus = blind Gymnophiona

•Tropical Distribution Characteristics: •Limbless (pectoral & pelvic girdles absent) •Degenerate Eyes (most are fossorial) •Internal Fertilization (phallodeum) •20% Viviparous; 80% Oviparous •Earthworm like (7 cm – 1.5 m) •6 Families Families: 1) Caeciliidae (Common Caecilians) 2) Ichthyophiidae (Fish Caecilians)

•95 species (57%) Dermophis mexicanus •38 species (23%) •Primary Annuli •Primary Annuli w/ •Most Fossorial Secondary & Tertiary •True tail •No true tail •Stegokrotaphic Skull •Stegokrotaphic Skull Ichthyophis kohtaoensis

Gymnophiona Families: 3) Typhlonectidae (Aquatic Caecilians) 4) Rhinatrematidae (Beaked Caecilians)

•14 species (8%) •9 species (5%) •Primary Annuli •Primary Annuli w/ Secondary •No true tail & Tertiary Grooves •Zygokrotaphic Skull •True tail Most Chthonerpeton indistinctum Primitive •Strongly Aquatic •Zygokrotaphic Skull

5) Scolecomorphidae (Tropical Caecilians) 6) Uraeotyphlidae (Indian Caecilians)

•6 species (4%) •5 species (3%) •Primary Annuli •Primary Annuli w/ •No true tail Secondary Grooves •Zygokrotaphic Skull •True tail •Vestigial scales in the •Stegokrotaphic Skull Scolecomorphus vittatus most posterior annuli Uraeotyphlus

Caudata •Smokeys Diversity (31) Characteristics: •Mostly Temperate Distribution •Tailed Amphibians •Well-developed limbs (except aquatic) •Internal Fertilization (most) •Larval Development External (most) •Lizard like (30 mm – 1.5 m) •Lack Tympanum & Middle Ear (opercular) •10 Families Families: 1) Plethodontidae (Lungless Salamanders) 2) Salamandridae (True Salamanders)

•378 species (68%) •74 species (13%) •U.S. & Neo-tropics •U.S., Europe, SE Asia •Cutaneous respiration •Lungs •Nasolabial groove •Skin toxic and brightly (chemoreception) colored •Reduced skull •Free-swimming larvae •Eggs usually guarded Plethodon shermani (most) Salamandra algira

3 Caudata Families: 3) Hynobiidae (Asian Salamanders) 4) Ambystomatidae (Mole Salamanders) •51 species (9%) •32 species (6%) •Asia •North America •Lack of courtship •Highly Terrestrial (most) (males deposit sperm) •Primarily Winter Breeders •Free-swimming larvae •Aquatic courtship •Teeth are in patches Hynobius chinensis •Free-swimming larvae Ambystoma tigrinum 5) Proteidae (Mudpuppies & Waterdogs) 6) Sirenidae (Sirens) •6 species (1%) •4 species (0.7%) •Eastern US & Europe •Southern US •Obligate Paedomorphic •Obligate Paedomorphic •Depressed body, external •External Fertilization gills (likely) •Necturus prefer crawfish •Pre-maxillary beak Necturus maculosus Siren intermedia

Caudata Families: 7) Rhyacotritonidae(Torrent Salamanders) 8) Dicamptodontidae (Giant Salamanders) •4 species (0.7%) •4 species (0.7%) •Coastal Pacific NW •Coastal NW and Canada •Semi-aquatic •Large living terrestrial •No operculum salamanders (20 cm SVL) •Reduced Lungs •Vomerine Teeth (M) •Bright yellow abdomen Rhyacotriton kezeri •Larvae develop 2-5 yrs Dicamptodon ensatus 9) Amphiumidae (Amphiumas) 10) Cryptobranchidae (Hellbenders)

•3 species (0.5%) •3 species (0.5%) •Eastern U.S. & China •SE United States •Obligate Paedomorphic •Obligate Paedomorphic •No external gills, gill slits •No external gills, gill slits •Excessive skin (respiration) •Spermatophore Directly •External Fertilization Deposited into Spermatheca Amphiuma tridactylum •Largest Salamanders in the Cryptobranchus •Number of Toes World (most primitive) alleganiensis

Anura Characteristics: •Shortened Presacral Vertebrate (usually 8) •Global Distribution Saltatorial •Ribs are reduced or absent (2nd or 4th) 2-10X BL •Presacral Vertebrae Firmly Articulated •Large Hind Limbs, No tail (except 1 family)

Video •External Fertilization (usually) •Flat heads and Large Mouths (usually) •Vocal Sacs in Males (usually) •29 Families Families: 1) Leptodactylidae (Southern Frogs) 2) Hylidae (Tree Frogs)

•1283 species (24%) •835 species (15%) N •Neo-tropics & subtropics •Global Distribution •Male broods eggs •Toes disks •E. jasperi is viviparious •Good climbers, jumpers (all other direct dev) •Free swimming tadpoles •Hawaii Eleutherodactylus coqui (most) Agalychnis callidryas

4 Anura Families: 3) Ranidae (True Frogs) 4) Bufonidae (True Toads) •799 species (14.7%) •493 species (9%) •Global (Bufo most spp.) •Global (Africa, Asia most) •Cutaneous Glands •Well-developed legs & •Teeth nearly absent webbed feet •Bidder’s Organ •Free swimming tadpoles Rudimentary Ovary on Testes (most) Rana catesbeiana Bufo cognatus 5) Microhylidae (Narrow-mouthed Frogs) 6) Rhacophoridae (Asian Tree Frogs)

•449 species (8%) •288 species (5%)

•Mostly Tropical, Sub- •Africa, India, SE Asia tropical •Hanging Foam Nest •2-3 Palatal Folds •“Flying Frogs” •Breviceps Secretions Stick to Female’s Back Gastrophryne carolinensis Rhacophorus reinwardtii

Anura Families: 7) Hyperoliidae (African Tree Frogs) 8) Dendrobatidae (Poison Arrow Frogs) •261 species (4.8%) •252 species (4.7%) •Central & South America •Africa, Madagascar, Seychelles •Brightly colored, toxic skin •Pupil vertically elliptical •Most very small (<1 inch) •Toe disks •Males wrestle for dominance •Reed and Sedge Frogs Leptopelis vermiculatus •Tadpoles ride on males back Dendrobates tinctorius

9) Mantellidae (Mantellas) 10) Centrolenidae (Glass Frogs)

•165 species (3%) •143 species (2.6%) •Madagascar only •Central & South America •Brightly colored, toxic skin •Transparent Skin (no ribs) •Most very small (<1 inch) •Most very small (<1 inch)

•Converged Evolutionarily with •Eggs guarded Dendrobatidae by males over Mantella madagascariensis stream Centrolene prosoblepon

Anura Families: 11) Megophryidae (Cryptic Frogs) 12) Myobatrachidae (Water Frogs) •138 species (2.5%) •126 species (2.3%) M •Asia & Indonesia •New Guinea, Australia, and Tasmania •Leaf-like Appearance •Poor Jumpers •Foam Nests in Water •Paddle Shaped Tongue •Rheobatrachus (extinct) •Tadpoles: Surface Foragers Brachytarsophrys carinensis Limnodynastes dumerilii 13) Arthroleptidae (Squeakers) 14) Pipidae (Tongueless Frogs) •51 species (0.9%) •31 species (0.6%) •Africa and South America •Sub-Saharan Africa •Fully Aquatic Frogs •Previously a part of Ranidae •Webbed feet, long fingers •Most lay eggs in water and with keratinized tips free-swimming tadpoles M •Eyes dorsal and no tongue Cardioglossa aureoli Xenopus laevis

5 Anura Families: 15) Astylosternidae (Astylosternids) 16) Discoglossidae (Disc-tongued frogs) •29 species (0.5%) •12 species (0.2%) A •Sub-Saharan Africa •Northern Africa, SW Europe •Often combined with #13 •Male carries eggs on hind legs •Differ from #13: horizontal •Females vocalize some pupils & toe discs •Toad-like (terrestrial & life •Hairy Frog Trichobatrachus robustus in burrows) Alytes obstetricans 17) Pelobatidae (Spadefoots) 18) Brachycephalidae (Pumpkin Toads)

•11 species (0.2%) •11 species (0.2%) •United States, Mexico, •SE Brazil Europe and Eastern Asia •All direct development •Xeric environments •Most bright orange •Explosive breeding M •B. didactylus: smallest tetrapod in southern •Fast developing larvae Scaphiopus couchii Brachycephalus ephippium Hemisphere (3/8”) (cannibalistic phenotype)

Anura Families: (Fire-bellied Toads (Shovel-nosed frogs) 19) Bombinatoridae & Barbourulas) 20) Hemisotidae •10 species (0.2%) •9 species (0.17%) A •Europe; Turkey, Russia, •Sub-Saharan Africa China, Korea, Japan •Burrows head first •Toxic Skin (unken reflex) •Lay eggs in burrow •Prehensile tongue •Barbourulas: Rocky streams Bombina orientalis Hemisus marmoratus 21) Heleophrynidae (Ghost Frogs) 22) Sooglossidae (Seychelles Frogs) •6 species (0.1%) •29 species (0.5%) •Southern Africa •Madagascar •Fast-flowing streams •Inguinal amplexus (only Neobatrachid ) •Well-developed toe discs, spines (males), oral disc •Secretive: litter and rocks (tadpoles) •Direct development & Sooglossus pipilodryas •Skeleton Gorge: Cape Town Heleophryne regis tadpoles on back

Anura Families: 23) Leiopelmatidae (Leiopelmatids) 24) Pelodytidae (Parley Frogs) •4 species (0.1%) •3 species (0.1%) A •Black & Caspian M •New Zealand Seas, S. Europe •Do not have protusible •Bulging Eyes; Parsley tongues Color •Do not call •Females reported Pelodytes punctatus •Alternating kicks (swim) Leiopelma archeyi vocalizing when amplexed (Mouth-brooding 25) Ascaphidae (Tailed Frogs) 26) Rhinodermatidae Frogs) •2 species (<0.1%) •2 species (<0.1%) •NW United States, A •Southern South British Columbia America (Chile) •Fast moving streams •Tadpoles Develop in •Tail: Cloacal Extension Vocal Sac (male) •Internal fertilization •“Rhinoceros nosed” •Most primitive extant family Ascaphus montanus Rhinoderma darwinii (don’t call, 7 yrs to maturation)

6 Anura Families: 27) Allophrynidae (Ruthven’s Frog) 28) Nasikabatrachidae (Purple Frog) •1 species (<0.1%) •1 species (<0.1%) •NE South America •India (discovered 2003) •Centrolenidae (related?) •Fossorial •Explosive breeders •Little known about its ecology •Little known Allophryne ruthveni Nasikabatrachus sahyadrensis 29) Rhinophrynidae (Mexican Burrowing Toad)

•1 species (<0.1%) •Costa Rica to Rio Grande •Fossorial •Explosive breeders •Ant-eating specialists M •No teeth Rhinophrynus dorsalis

Fossil Record of Amphibians

First Amphibians Modern Mississippian Epoch Amphibians 350 MYA (late Permian) 250 MYA

Carboniferous

Lobe-finned or Lungfishes? Origin of Tetrapods Lobe-finned Fish Lungfish (Osteolepis) (Rhipidistia)

Fin-fold vs. body-spine theories

Neoceratodus forsteri •Freshwater & Marine •Marine (Freshwater) •Lungs & Gills •Lungs & Gills •Ovoviparious •Similar Skeleton, Lungs, •Dentition, Mouth Parts Circulatory System

Labyrinthodont amphibians Fossil Record Ontogeny & Anatomy (Ichthyostega) (extant)

7 Fish to Tetrapods Greenland Late Devonian Period 360 MYA

Ichthyostega Acanthostega

1 m 0.6 m

•Piscivorous •Piscivorous •Limbs likely used •Fish-like for navigating •Limbs likely used •Tail for balance for paddling •Skeletal structure •Skeletal structure ¾forelimbs ¾Elbow could not bend •Lungs •Gills and Lungs

First Tetrapods Carboniferous and Permian Periods Labyrinthodontia Lepospondyli

Anthracosauria Temnospondyli Aistopoda Nectridea Microsauria

1) Embolomeri 1) Trematosauroidea 2) Seymouridae 2) Eryopoidea 3) Dissorophidae (biphasic) Anurans Salamanders Caecilians Lissamphibia (Monophyletic Origin) Lissamphibia (Polyphyletic) Paedomorphism

Temnospondylous Amphibians Carboniferous and Permian Periods •1.5-2 m long •Bicuspid pedicellate teeth •Tympanum likely

•Lungs & Cutaneous Respiration

•Likely piscivorous Eryopus megacephalus •Engulfed prey

•Not a strong swimmer or fast tetrapod (likely hunted by stealth or opportunity)

•Shoulder disconnected from skull

8 Nectrideans and Microsaurs Carboniferous and Permian Periods

Nectridia •Mostly Aquatic •Resembled Newts (flat tails) •Some with triangular heads •Hydrofoils in slow moving Jurassic (180 mya) streams •Small fish and aquatic Microsauria 0.5-1 m invertebrates •“Small Lizard” •Terrestrial (lizards), aquatic (newts), and Diplocaulus magnicornus fossorial

Fossil Record of Lissamphibia Probably Triassic Triassic, Jurassic and Cretaceous Periods for All Orders 2) Salamanders 1) Anurans 3) Caecilians Video Paleobatrachus What are the most primitive families? 14 Geotrypetes seraphini Triadobatrachus massinoti Karuaus sharovi Apodops pricei •Origin: Madagascar •Origin: Kazakstan •Origin: Gondwanaland (SA) •Early Triassic (230 mya) •Late Jurassic (170 mya) •Late Cretaceous (100 mya)

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