Lissamphibia ~4,900 species

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

Lissamphibia Gymnophiona (caecilians)

Typhlonectes

Typhlonectes

CAECILIANSThe 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)

Fig. 3-11 Pough et al. 2001

Fossil Gymnophiona ancestor (Eocaecilia)

evidence of tentacles

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)

zygokrotaphic = skull weak in temporal region

Lots of bones fused

stegokrotaphic = skull completely roofed

stegokrotaphic

Fig. 3-10 Pough et al. 2001

Fig. 13-12 Duellman and Trueb, 1986

Fig. 13-15 Duellman and Trueb, 1986

Caecilian skulls vs. Anuran skullZ

S

G

S S

S S

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. Fossorialanimals 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 EmbryoEmbryo removed fromegg. Yolk is visible aswell as sensory structures along headand side of body. These include mechano- and electrical receptorsof the lateral line.Eggs are laid inburrows near streams.hatch, larval stage livesin streams until metamorphosis a yearlater.

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. 5-5 Duellman and Trueb, 1986

Fig. 17-13 Stebbins and Cohen, 1995

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.

Toxic glands

Mucus 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

Fig.3-12 Pough et al. 2001

Lissamphibia Gymnophiona (caecilians) 6 families, 34 genera, 165 spp.

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 MarvaleeH. 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)

Ichthyophiidae2 Genera, 38 species+; SE Asia, India, Islands of

the Indo-Pacific, and the PhilippinesTerrestrialOvivparous (up to 100 eggs)True TailTentacle closer to eye than nostril500 mmStegokrotaphic skullDermal 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 soldin fish stores.Aquatic.Female withyoung.

Typhlonectidae

• Aquatic caecilian, viviparous

• Larval gills

Ambystoma californiense

Lissamphibia Urodela

(salamanders) 10 families, 61 genera, 415 spp.

Ambystoma californiense

Ambystoma tigrinum

Unken reflexFig. 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)

mental glands

Fig. 17.3 Stebbins and Cohen, 1995

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

(via spermatophore)

Duellman and Trueb, 1986

female

male

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

Sala

man

der

Larv

ae

Pond

Stream

Terrestrial

Stebbins and Cohen, 1995

Urodela (salamanders) - Paedomorphosis common

all adults retain larval characteristics

OR some retain larval characteristics

(facultative) OR

none retain larval characteristics - makes phylogenetic reconstruction difficult

Urodela (salamanders)

- Unique defensive

adaptations Duellman and Trueb, 1986

Fig. 10-7 Duellman and Trueb, 1986

Urodela (salamanders) - Unique defensive adaptations

Fig. 3-1 Pough et al. 2001

Lissamphibia Urodela

(salamanders) 10 families, 61

genera, 415 spp.

Fig. 10-7 Duellman and Trueb, 1986

Urodela (salamanders) - Unique defensive adaptations

Echinotriton chinhaiensis Chinhai Salamander Salamandridae © Max Sparreboom

Urodela

Pough et al. 2001

Sirenidae Hynobiidae

Salamandridae

Pough et al. 2001

Urodela

Urodela

PlethodontidaeProteidae

Pough et al. 2001

Urodela (salamanders) Sirenidae

(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)

Urodela (salamanders) Cryptobranchidae

(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)

The Hellbender Cryptobranchus alleganiensis (photo M.A. Donnelly)

© Dr. Eric J. Routman

Urodela (salamanders) Hynobiidae

(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

Urodela (salamanders) Amphiumidae

(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

Urodela (salamanders) Plethodontidae

(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

Fig.3-6 Pough et al. 2001

Plethodontidae

Figs 7.2 and 6.1 Stebbins and Cohen, 1995

Urodela (salamanders) Rhyacotritonidae

(1 genus, 4 species; Pacific Northwest U.S.)

- inhabit old-growth forest (indicator species)

- very old lineage

Rhyacotriton olympicus Olympic Torrent Salamander © William Flaxington

Urodela (salamanders) Proteidae

(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

Urodela (salamanders) Salamandridae

(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)

Fig. 13.5 Stebbins and Cohen, 1995

- defensive displays - aposematic coloration

(bright warning) - tetrodotoxins (neuro)

Unken reflex

Newts Taricha spp.

Salamandra salamandra Fire Salamander © Arie van der Meijden

Taricha granulosa Rough-skinned Newt © Harry Greene

Urodela (salamanders) Ambystomatidae

(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

Urodela (salamanders) Dicamptodontidae

(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

Lissamphibia

Anura (frogs)

~28 families, 310 genera, 4,300 spp.

Fig. 3-20 Pough et al. 2001

Zug et al. 2001

caecilian

salamander

frog

Anura (frogs) (see Pough CH3) - Salientia (clade that includes extinct

Triadobatrachus)

Pough et al. 2001

tail

extra vertebrae

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

Stebbins and Cohen, 1995

Derived jumper

Likely ancestral state was terrestrial protofrog that moved into water in riparian system to avoid danger.

‘Jumping’ is fast way to get to safety.

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

Fig. 3-16 Pough et al. 2001

- 9 or fewer vertebrae

- fused bones limbs, urostyle

- no tail

- elongate hindlimbs ankles, feet

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

Stebbins and Cohen, 1995

Eggs deposited: - in water - on land - suspended in air

Development: - complete metamorphosis - direct development - viviparity

Anura (frogs)

Reproduction Parental Care:

not typical, but...

Stebbins and Cohen, 1995

Stebbins and Cohen, 1995

Darwin frog, vocal sac

Anura (frogs) Reproduction Metamorphosis:

Tadpole (Larvae) - herbivorous filter feeders - some carnivorous - or cannibalistic - some don’t feed at all

Stebbins and Cohen, 1995

Modify gut, body plan, mouth, jaws, limbs etc.

Adult - mostly carnivorous - two frugivorous species - tongue attachment

Lissamphibia

Anura (frogs)

~28 families, 310 genera, > 4,300 spp.

Fig. 3-20 Pough et al. 2001

Anura (frogs)

Larvae

Stebbins and Cohen, 1995

Stebbins and Cohen, 1995

Surface film

Suctorial scraper

Carnivore

Use to ID

Internal Gills

Anura (frogs)

Larvae General types based on morphology and diet

1 2 3 4

Pough et al., 2001

spiraclespiracles

Keratinous mouth parts

Anura (frogs)

SoundMost 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.

glands - mucus (2 types) - poison = granular pigmentation

Fig 2.1 Stebbins and Cohen, 1995

12

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

Stebbins and Cohen, 1995

Pigmentation under hormonal control

-reflectance -infrared -aposematic

Anura (frogs) Skin

Respiration - blood vessels

Stebbins and Cohen, 1995

- epidermal thickness

- versus hydration gas transfer requires ‘solution’

Lissamphibia

Anura (frogs)

~28 families, 310 genera, 4,300 spp.

Fig. 3-20 Pough et al. 2001

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

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 hochstetteri

Leiopelma hamiltoni

Anura (frogs) Bombinatoridae

(2 genera, 8 species; Europe, E Asia)

- Bombina toxic skin secretions aposematic coloration (~orange + yellow) unken reflex

Bombina orientalis

Lissamphibia

Anura (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

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

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

Lissamphibia

Anura (frogs)

~28 families, 310 genera, 4,300 spp.

Fig. 3-20 Pough et al. 2001

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

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

Anura (frogs) Myobatrachidae

(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

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

Anura (frogs) Hylidae

(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

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 oyampiensis

Centrolenella fleischmanni

Lissamphibia

Anura (frogs)

~28 families, 310 genera, 4,300 spp.

Fig. 3-20 Pough et al. 2001

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

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

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

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

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