Lissamphibia ~4,900 species (more than number of extant mammal species) >4,300 species frogs (Anura) >415 species salamanders (Urodela) >165 species caecilians (Gymnophiona)

Gymnophiona (caecilians) Lissamphibia Gymnophiona (caecilians) Typhlonectes Typhlonectes

CAECILIANS The Unknown Amphibian

Who are they? Order: Gymnophiona Family: 6 families Genus: 34 Species: 165 Habitat: loose soil, leaf litter in tropical forests or rivers and streams Length: up to 2.4m; shortest 3.5 in. Up to 2.2 lbs Life span: up to 13 yrs Offspring: 30 – 60 eggs; 2 - 25 young born

Range Central Africa, Southeast Asia, Southern Mexico to Argentina

Description Caecilians are tropical amphibians that look like large worms or slick snakes. They have no arms or legs, and sometimes it’s hard to tell which end is the head and which is the tail! Their shiny skin is ringed with skin folds called annuli, and they usually come in shades of gray, brown, black, orange, or yellow. Some species have tiny, fishlike scales (dermal scales) within the rings.

Gymnophiona (caecilians) (see Pough CH3) - elongate, distinctly annulated -primary etc. - terrestrial, burrowing, or aquatic (derived) - tails reduced or absent - eyes reduced (covered by skin or even bone) - limbs and girdles absent in all extant taxa (still present in fossil ancestor)

Fossil Gymnophiona ancestor evidence of tentacles Fossil Gymnophiona ancestor (Eocaecilia) Fig. 3-11 Pough et al. 2001

Annuli and Smooth

Dermal Scale Present in Some Caecilians

Gymnophiona (caecilians) dermal scales in some spp. - pouches in dermis below annular groove - scales like this not found in other Lissamphibia Fig. 3-9 Pough et al. 2001

Caecilian Head

Gymnophiona (caecilians) - Skulls unique - Well ossified (but openings for eyes, nares, tentacles) stegokrotaphic = skull completely roofed zygokrotaphic = skull weak in temporal region vs. gymokrotaphic = temporal region open (anurans + urodelans)

skull completely roofed stegokrotaphic = skull completely roofed zygokrotaphic = skull weak in temporal region stegokrotaphic Fig. 3-10 Pough et al. 2001 Lots of bones fused

Caecilian skulls vs. Anuran skull Z S S S G S S Fig. 13-15 Duellman and Trueb, 1986 Fig. 13-12 Duellman and Trueb, 1986

Gymnophiona (caecilians) - many bones of skull fused - Why have well ossified skull? - unique dual jaw closing mechanism

Fossorial Adult caecilian can bury itself in a matter of minutes. Fossorial animals spend most of their time underground.

Aquatic Species

Gymnophiona (caecilians) - left lung often reduced or absent - aquatic eggs and larvae, or terrestrial oviposition with female parental care - some species viviparous - internal fertilization (phallodeum)

Male Typhlonectes (cloaca) Typhlonectes (mating)

Oviparous Species Some female caecilians lay eggs in damp holes near water. When the larvae hatch they have gills and a short, finned tail to help them swim in the water, feeding on plankton. Through a series of changes the gills are replaced by a single lung, the skin becomes thicker, the annuli develop, and sensory tentacles appear. At this point the newly developed adult returns to the land and goes underground.

Caecilian Embryo Embryo removed from egg. Yolk is visible as well as sensory structures along head and side of body. These include mechano- and electrical receptors of the lateral line. Eggs are laid in burrows near streams. hatch, larval stage lives in streams until metamorphosis a year later. Icthyophis kohtaoensis

Viviparous Species Some species give birth to live young that are fully developed inside the mother before they are born.

Gymnophiona (caecilians) In viviparous species, - young nourished by secretions from oviduct - mother’s skin may produce edible secretions after birth

Fig. 17-13 Stebbins and Cohen, 1995 Fig. 5-5 Duellman and Trueb, 1986

Larval Caecilian Aquatic stage with gills that are transient.

Senses A hard, thick, pointy skull helps these amphibians dig in soft dirt. Because of their underground lifestyle, caecilians have little need to see or hear. Therefore, their eyes are very tiny in some species, or hidden under the skin or skull in other species, making just tiny gray bumps for eyes. Some species in South America spend their lives in water instead of on land. Caecilians don’t have ear openings, so it is doubtful they can hear sounds.

Tentacles Tentacles, located between the nostrils and the eyes, are used to locate prey and detect surroundings.

Gymnophiona (caecilians) TENTACLE - chemoreception - between eyes and nostrils - protrusible in some taxa - involves structures normally associated with eye and Jacobsen’s organ

Diet Inside a caecilian’s mouth are dozens of needle-sharp teeth. The teeth are used to grab worms, termites, beetle pupae, mollusks, small snakes, frogs, lizards, and even other caecilians. All food is swallowed whole.

Eating tubifex worms

Skin Glands Caecilians have toxic glands in their skin that sometimes protect them from being eaten by other animals. Mucus glands Toxic glands

Families of Caecilians Rhinatrematidae South America Ichthyophiidae Southeast Asia Uraeotyphlidae Southern India Scolecomorphidae Subsahara Africa Caeciliaidae South and Central America, Subsahara Africa, Southern Asia Typhlonectidae South America

Gymnophiona Pough et al. 2001

Lissamphibia Gymnophiona (caecilians) 6 families, 34 genera, 165 spp. Fig.3-12 Pough et al. 2001

Gymnophiona (caecilians) Rhinatrematidae (2 genera, 9 species; northern South America) - ancestral (‘primitive’) lineage - true tail - mouth at tip of snout - tentacle next to eye - zygokrotaphic skull (weaker) - many scales - not well-known - likely not fossorial - relatively small - oviparous (egg-laying), with aquatic larvae

Rhinatrematidae Small, terrestrial caecilian with aquatic larvae @1998 Marvalee H. Wake

Gymnophiona (caecilians) Uraeotyphlidae 1 genus, 5 species; Southern India Stegokrotaphic skulls oviparous (with aquatic larvae) small (300 mm) true tail Tentacle underneath the nostril

Uraeotyphlidae

Gymnophiona (caecilians) Ichthyophiidae 2 Genera, 38 species+; SE Asia, India, Islands of the Indo-Pacific, and the Philippines Terrestrial Ovivparous (up to 100 eggs) True Tail Tentacle closer to eye than nostril 500 mm Stegokrotaphic skull Dermal Scales

Ichthyophiidae Large terrestrial caecilian with aquatic larvae

Gymnophiona (caecilians) Scolecomorphidae (2 genera, 5 species; parts of central Africa) - unusual lineage - vestigial eyes attached to tentacles - orbits absent - zygokrotaphic skull lacking elements - calcified spines on male phallodeum - no scales - oviparous or viviparous

Scolecomorphidae

Gymnophiona (caecilians) “Caeciliidae” (21 genera, 90 species; central and S. America, parts of Africa and Asia) - no tail - mouth recessed under snout - tentacular location varies - scales variable - mostly burrowers - wide range of sizes - some brightly colored - life history variable

Caeciliaidae Very varied with small (10cm) to large (1.5m) organisms. Terrestrial, aquatic, oviparous, viviparous. Most are gray – black but some are more colorful.

Gymnophiona (caecilians) Typhlonectidae (5 genera, 13 species; South America) - often aquatic - tracheal lungs - narial plugs - secondarily zygokrotaphic skulls - includes largest lungless tetrapod - nocturnal - viviparous with aquatic larvae

Typhlonectes Sometimes sold in fish stores. Aquatic. Female with young.

Typhlonectidae Aquatic caecilian, viviparous Larval gills

Ambystoma californiense

Lissamphibia Urodela (salamanders) 10 families, 61 genera, 415 spp. Ambystoma tigrinum Ambystoma californiense Unken reflex Fig. 13.5 Stebbins and Cohen, 1995

Urodela (salamanders) (see Pough CH3) - Urodela (extant) - Caudata (extant plus fossil relatives) - North America and temperate Eurasia - Plethodontids have radiated in tropics - extensive salamander fossil record (unlike Gymnophiona)

Urodela (salamanders) - typically 4-limbed, short bodied, long tail some with limbs reduced or lost - costal grooves - most species terrestrial, but need water for reproduction (some fully aquatic or terrestrial) - some arboreal

Urodela (salamanders) - unique jaw musculature - skulls reduced (bones absent) - skull bone ossification sequence - late appearance of maxillae in skull

Urodela (salamanders) - lack middle ear cavities and tympana (drum) - various opercular components missing Pough et al. 2001

Urodela (salamanders) - mucous and poison glands (pheromones) - aggregations of mucous glands = courtship glands (e.g., mental glands)

Fig. 17.3 Stebbins and Cohen, 1995 mental glands

Urodela (salamanders) - some external fertilization - mostly internal fertilization (via spermatophore)

female male Duellman and Trueb, 1986

Urodela (salamanders) - large genomes (and large cell nuclei) - usually have larval stage larvae with true teeth, gill slits, external gills - larvae rather similar to adults (compared to anurans) palate is remodelled during metamorphosis - many with direct development

Pond Stream Salamander Larvae Terrestrial Stebbins and Cohen, 1995

Urodela (salamanders) - Paedomorphosis common all adults retain larval characteristics OR some retain larval characteristics (facultative) none retain larval characteristics - makes phylogenetic reconstruction difficult

Urodela (salamanders) - Unique defensive adaptations Duellman and Trueb, 1986

Urodela (salamanders) - Unique defensive adaptations Fig. 10-7 Duellman and Trueb, 1986

Lissamphibia (salamanders) Urodela 10 families, 61 genera, 415 spp. Fig. 3-1 Pough et al. 2001

Urodela (salamanders) - Unique defensive adaptations Fig. 10-7 Duellman and Trueb, 1986 Echinotriton chinhaiensis Chinhai Salamander Salamandridae © Max Sparreboom

Urodela Pough et al. 2001 Sirenidae Hynobiidae Salamandridae

Urodela Pough et al. 2001

Urodela Plethodontidae Proteidae Pough et al. 2001

Sirenidae Urodela (salamanders) - ancestral lineage (2 genera, 4 species; SE U.S., NE Mexico) - ancestral lineage (sister to all other salamanders) - long, slender, eel like - lack pelvic girdle and hindlimbs - keratinized beak - fully aquatic - prey on invertebrates (insects, crayfish, worms) - Paedomorphic (no eyelids, external gills, non-pedicillate teeth, reduction in number of digits on forelimbs) - mucous cocoon and aestivation - external fertilization? - oviparous The dwarf-siren Pseudobranchus striatus (photo J. White)

Cryptobranchidae Urodela (salamanders) - incomplete metamorphosis (2 genera, 3 species; Japan, China, E N. America) - incomplete metamorphosis adults lack eyelids, retain one pair gill slits - flattened bodies and heads - aquatic - asymmetrical suction feeding - cutaneous respiration - largest salamanders (up to 1.8 m) - cold mountain streams - external fertilization - males make nests and guard eggs (Den Master) © Dr. Eric J. Routman The Hellbender Cryptobranchus alleganiensis (photo M.A. Donnelly)

Hynobiidae Urodela (salamanders) - complete metamorphosis (7 genera, 36 species; disjunct Asia) - complete metamorphosis eyelids, lack gill slits as adults - lungs may be reduced or absent - some fully aquatic - some with terrestrial adults and migration to breed - relatively small (100-250 mm) - some breed while wetlands still ice and snow covered - males have territories - males may compete (mating ball) - external fertilization Batrachuperus mustersi Photo by Max Sparreboom

Amphiumidae Urodela (salamanders) (1 genus, 3 species; S, SE U.S.) - elongate, paedomorphic lack eyelids, lack external gills (but have slits) - pedicellate teeth - retain both pairs of limbs (and girdles), but small limbs - aquatic - eat invertebrates and vertebrates - ocassionally move overland or aestivate - up to 1.1 m long - internal fertilization - oviparous on land (alligator nest mounds?) female parental care Two-toed amphiuma Amphiuma means © John White

Plethodontidae Urodela (salamanders) (28 genera, 266 species; disjunct N, Central, S America, ~ Italy) - diverse and specious (only group to radiate in tropics) - lungless (adaptation to mountain streams) - nasolabial groove (chemoreception) - subterranean, aquatic, terrestrial, arboreal - variable body forms (arboreal often with webbed feet and prehensile tails) - variable life history strategies - include smallest and ~largest terrestrial Urodela Batrachoseps stebbinsi Tehachapi Slender Salamander © Tim Manolis

Plethodontidae Figs 7.2 and 6.1 Stebbins and Cohen, 1995 Fig.3-6 Pough et al. 2001

Rhyacotritonidae Urodela (salamanders) - inhabit old-growth forest (1 genus, 4 species; Pacific Northwest U.S.) - inhabit old-growth forest (indicator species) - very old lineage Rhyacotriton olympicus Olympic Torrent Salamander © William Flaxington

Proteidae Urodela (salamanders) - diploid chromosome count of 38 (2 genera, 6 species; NE U.S., S Central Europe) - diploid chromosome count of 38 - paedomorphic large gills and caudal fins - lack maxillary (~upper jaw) bone - mostly aquatic - Proteus live in caves (slender; whitish skin; reduced eyes) Proteus anguinus

Salamandridae Urodela (salamanders) (15 genera, 55 species; N America, Europe, Asia, N Africa) - includes ‘newts’ - may have extremely rugose skin - life history variable - some species with efts (terrestrial immature) Taricha granulosa Rough-skinned Newt © Harry Greene Unken reflex Newts Taricha spp. Fig. 13.5 Stebbins and Cohen, 1995 - defensive displays - aposematic coloration (bright warning) - tetrodotoxins (neuro) Salamandra salamandra Fire Salamander © Arie van der Meijden

Ambystomatidae Urodela (salamanders) (1 genus, 32 species; N America) - several hybrids and unisexual forms variable ploidy and number of parental species - hybrids generally of ancient origin - Ambystoma mexicanum often used in research - variable metamorphosis (none, some, all) - robust and ‘medium sized’ Ambystoma californiense

Dicamptodontidae Urodela (salamanders) (1 genus, 4 species; ~NW U.S.) - similar to Ambystomatidae - relatively large - inhabit coniferous forest habitats cold streams and cold mountain lakes - species very difficult to differentiate morphologically Dicamptodon tenebrosus Pacific Giant Salamander © Henk Wallays

Rana pipiens

Anura Lissamphibia (frogs) ~28 families, 310 genera, 4,300 spp. Fig. 3-20 Pough et al. 2001

caecilian salamander frog Zug et al. 2001

Anura (frogs) (see Pough CH3) - Salientia (clade that includes extinct Triadobatrachus) extra vertebrae tail Pough et al. 2001

- most extant families first appear in the Cretaceous Anura (frogs) - most extant families first appear in the Cretaceous - radiation in the early Cenozoic Ascaphus truei

Anura (frogs) (see Pough CH3) GENERAL - tail absent - metamorphosis larvae and adults very different - specialized skin... - jumpers (saltation) - 88% of Lissamphibia are Anura - found ~worldwide except Antarctica, poles, and very dry deserts

Anura (frogs) Jumping Most anurans jump Likely ancestral state was terrestrial protofrog that moved into water in riparian system to avoid danger. ‘Jumping’ is fast way to get to safety. Derived jumper Stebbins and Cohen, 1995

Anura (frogs) Jumping (lose mass, add rigidity) - inflexible vertebral column - caudal vertebrae fused to form urostyle - loss and reduction of skull bones - loss of teeth in lower jaw (except one species) - anterior ribs reduced or lost - radius-ulna and tibia-fibula fused - elongate ankle bones (astragulus-calcaneum) transfers energy to trunk during push-off - limbs folded under body (greater propulsion)

Anura (frogs) Jumping etc. - skull reduced - 9 or fewer vertebrae - fused bones limbs, urostyle - no tail - elongate hindlimbs ankles, feet Fig. 3-16 Pough et al. 2001

Anura (frogs) Pectoral Girdles 1. arciferal - widespread - ancestral 2. firmisternal - derived - systematics - intermediate conditions - reversals

Anura (frogs) Reproduction (typically external) Amplexus: 1. inguinal 2. axillary ------> 3. cephalic Eggs deposited: - in water - on land - suspended in air Stebbins and Cohen, 1995 Development: - complete metamorphosis - direct development - viviparity

Anura (frogs) Reproduction Parental Care: not typical, but... Darwin frog, vocal sac Stebbins and Cohen, 1995 Stebbins and Cohen, 1995

Anura (frogs) Reproduction Metamorphosis: Tadpole (Larvae) - herbivorous filter feeders - some carnivorous - or cannibalistic - some don’t feed at all Stebbins and Cohen, 1995 Adult - mostly carnivorous - two frugivorous species - tongue attachment Modify gut, body plan, mouth, jaws, limbs etc.

~28 families, 310 genera, > 4,300 spp. Lissamphibia Anura (frogs) ~28 families, 310 genera, > 4,300 spp. Fig. 3-20 Pough et al. 2001

Anura (frogs) Larvae Surface film Internal Gills Suctorial scraper Stebbins and Cohen, 1995 Suctorial scraper Carnivore Use to ID Stebbins and Cohen, 1995

Anura (frogs) Larvae General types based on morphology and diet 1 2 3 Keratinous mouth parts 1 2 3 4 spiracles spiracle Pough et al., 2001

Anura (frogs) Sound Most important anuran communication tool - Most anurans vocalize - Usually male - Inflate throat sacs - species specific calls - mate attraction - territoriality - alarm calls - more later...

Anura (frogs) Skin Specialized for multiple functions - hydration, defense, locomotion, thermoregulation, reproduction, respiration etc. 2 1 glands - mucus (2 types) - poison = granular pigmentation Fig 2.1 Stebbins and Cohen, 1995

Anura (frogs) Skin Specialized glands A. mucus -1 moist coating prevent dehydration -2 sexual dimorphism nuptial pads Nuptial pads Pough et al., 2001 B. poison = granular -defensive secretions (sticky, antibiotics, toxic, etc.) Dendrobates tinctorious

Anura (frogs) Skin Pigmentation (Chromatophores) Xanthophores Iridophores Melanophores -reflectance -infrared -aposematic Stebbins and Cohen, 1995 Pigmentation under hormonal control

Anura (frogs) Skin Respiration - blood vessels - epidermal thickness - versus hydration gas transfer requires ‘solution’ Stebbins and Cohen, 1995

Anura Lissamphibia (frogs) ~28 families, 310 genera, 4,300 spp. Fig. 3-20 Pough et al. 2001

(1 species; ~NW U.S., into Canada) Anura (frogs) Ascaphidae (1 species; ~NW U.S., into Canada) - monotypic Family and Genus - ‘tailed frog’ - tail is extension of cloaca - internal fertilization (1 of ~3 spp.) - do not call - no tympana - highly turbulent aquatic habitat Ascaphus truei

(1 genus, 3 species; New Zealand) Anura (frogs) Leiopelmatidae (1 genus, 3 species; New Zealand) - only amphibians native to NZ - ribs embedded in ventral musculature - lack ear components and vocal sac - direct development - male parental care in 2/3 species Leiopelma hamiltoni Leiopelma hochstetteri

(2 genera, 8 species; Europe, E Asia) Anura (frogs) Bombinatoridae (2 genera, 8 species; Europe, E Asia) - Bombina toxic skin secretions aposematic coloration (~orange + yellow) unken reflex Bombina orientalis

Anura Lissamphibia (frogs) ~28 families, 310 genera, 4,300 spp. Fig. 3-20 Pough et al. 2001

Anura (frogs) Pelobatidae (3 genera, 11 species; N America, Eurasia) - include ‘spade foots’ - well-developed keratinous, spade-like metatarsal tubercle on hind feet - fossorial - often with enlarged parotoid glands on dorsum - desert adapted aestivate explosive breeders egg to metamorph in ~8 days

Anura (frogs) Pelobatidae (con’t) Scaphiopus couchii spade

(1 species; Texas to Costa Rica) Anura (frogs) Rhinophrynidae (1 species; Texas to Costa Rica) - monotypic family and genus - ultra fossorial spade tubercles pointed head with cornified skin small eyes no tympanum reinforced skull - feed on ants and termites underground - unique tongue Rhinophrynus dorsalis

(5 genera, ~30 species; Panama, S America, sub-Saharan Africa) Anura (frogs) Pipidae (5 genera, ~30 species; Panama, S America, sub-Saharan Africa) - no tongue - keratinous ‘claws’ - aquatic - modified ears and calling - Xenopus laevis research polyploids - Pipa spp. eggs in dorsal skin of female X. tropicalis

Anura Lissamphibia (frogs) ~28 families, 310 genera, 4,300 spp. Fig. 3-20 Pough et al. 2001

(33 genera, ~400 species; widespread, not in Australopapuan region) Anura (frogs) Bufonidae (33 genera, ~400 species; widespread, not in Australopapuan region) - Bidder’s organ rudimentary ovary on male testes (paedomorphic) - no teeth - parotoid glands toxins - Bufo marinus pest

(49 genera, > 900 species; Americas, West Indies) Anura (frogs) “Leptodactylidae“ (49 genera, > 900 species; Americas, West Indies) - not monophyletic - variable - Eleutherodactylus > 500 species!! most species rich genus of vertebrates some with direct dvpt. 2 spp. with internal fert. Eleutherodactylus auriculatus Ceratophrys cornuta

Myobatrachidae Anura (frogs) - variable - one species with (21 genera, 120 species; Australia, New Guinea, Tasmania) - variable - one species with male inguinal pouches for brood rearing - two species with gastric brooding in female Rheobatrachus (extinct?) Rheobatrachus vitellinus

(2 species; Argentina and Chile) Anura (frogs) Rhinodermatidae (2 species; Argentina and Chile) - fleshy proboscis at tip of snout - males carry larvae to water, or brood in vocal pouch Rhinoderma darwinii

Hylidae Anura (frogs) - arboreal generally - well-developed toe discs (38 genera, 760 species; Americas, W indies, Australopapuan region) (Hyla in Americas, Eurasia, Japan, N Africa) - arboreal generally - well-developed toe discs - claw-shaped terminal phalanges - many spp. with females that transport young dorsally - Phyllomedusa toxin for native rituals lipid glands in skin wiping behavior Phyllomedusa sauvagi

(3 genera, > 130 species; Mexico to S America) Anura (frogs) Centrolenidae (3 genera, > 130 species; Mexico to S America) - medial process on 3rd metacarpal - toe discs - terminal phalanges T-shaped - eggs attended by males - transparent venter = ‘glass frogs’ Centrolenella fleischmanni Centrolenella oyampiensis

Anura Lissamphibia (frogs) ~28 families, 310 genera, 4,300 spp. Fig. 3-20 Pough et al. 2001

(6 genera, 185 species; Cent. America, N South America) Anura (frogs) Dendrobatidae (6 genera, 185 species; Cent. America, N South America) - pair of dermal scutes on dorsal surface of fingers - generally diurnal and terrestrial - cephalic amplexus (if amplex) - parental care move larvae around - Dendrobates may feed tadpoles eggs - Phyllobates terribilis lipophilic alkaloids dietary origin Dendrobates tinctorious

(7 genera, 75 species; sub-Saharan Africa) Anura (frogs) Arthroleptidae (7 genera, 75 species; sub-Saharan Africa) - includes Trichobatrachus robustus (hairy frog) male sits on clutch and aids aeration? Stebbins and Cohen, 1995

(46 genera, > 700 species; most everywhere, except many islands) Anura (frogs) “Ranidae” (46 genera, > 700 species; most everywhere, except many islands) - likely not monophyletic - variable - some unique Rana esculenta hybrids both sexes represented alternate generations sexual <---> asexual Rana pipiens

(19 genera, 230 species; sub-Saharan Africa, Seychelles, Madagascar) Anura (frogs) Hyperoliidae (19 genera, 230 species; sub-Saharan Africa, Seychelles, Madagascar) - many arboreal - toe discs - ~ brightly colored - Afrixalus eggs on leaf then ‘taco’ Afrixalus osorioi congicus

(15 genera, 315 species; Africa, Madagascar, Asia) Anura (frogs) Rhacophoridae (15 genera, 315 species; Africa, Madagascar, Asia) - mostly arboreal - enlarged toe discs - some with foam nests - some communal nests - Mantella with skin alkaloids and aposematic coloration Buergeria japanicus