Herpetology – the study of amphibians and reptiles

• Both are very diverse groups and are as different from one another as are birds and mammals

• Why study them collectively?

– Traditionally, they’ve been studied together because of complimentary life histories and the same or similar study techniques can be used in the field and laboratory

– Also, it may have something to do with historical lack of interest in studying these groups because of:

• Relative small size and secretive nature (among vertebrates)

• Lack of commercial value

• Un-endearing qualities (i.e., they’re creepy and slimy to some folks, even some biologists)

– There is no indication that herpetology may become two separate fields of study

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1 Vertebrate Evolution

• Phylum Chordata characteristics – may be with organism its entire life or only during a certain developmental stage

1. Dorsal, hollow nerve cord

2. Flexible supportive rod (notochord) running along dorsum just ventral to nerve cord

3. Pharyngeal slits or pouches

4. A tail during some point of development

• Phylum Chordata has 3 subphyla 1. Urochordata – tunicates; adults are sessile marine animals with gill slits • Larvae are free-swimming and possess notochord and nerve cord in muscular tail • Tail is reabsorbed when larvae transforms into an adult

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2 2. Cephalochordata –lancelets; small marine animals that live in sand in shallow water • Retains gill slits, notochord, and nerve cord thru life

3. Vertebrata – chordates with a “backbone”; persistent notochord, or vertebral column of bone or cartilage • All possess a cranium

• All embryos pass thru a stage when pharyngeal pouches are present

• Recently, Vertebrata has been changed to Craniata with 3 superclasses: Myxini (hagfish), Petromyzontida (lampreys) and Gnathastomata (jawed vertebrates)

Lamprey ammocoete

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3 Jawless Fish

Lamprey Hagfish

Vertebrate Evolution 1. Tunicate larvae

2. Lancelet

3. Larval lamprey (ammocoete) and jawless fishes

4. Jaw development from anterior pharyngeal arches – capture and ingestion of more food sources

5. Paired fin evolution A. Eventually leads to tetrapod limbs B. Fin spine theory – spiny sharks (acanthodians) had up to 7 pairs of spines along trunk and these may have led to front and rear paired fins

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4 • Emergence onto land

– Extinct lobe-finned fishes called rhipidistians seem to be the most likely tetrapod ancestor

• Similar to modern lungfish, had gills and probably lungs to breathe air

• Teeth and limb bones closely resemble early amphibian bones

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5 – Modern “walking” fish include walking catfish, mudskippers, and lungfish

Lungfish – found in South Mudskipper America, Africa, and Australia

Walking catfish – from southeast Asia but now found in Florida

– Earliest known amphibians were labyrinthodonts

• Had traits of lobe-finned fish and later tetrapods • Most modern salamanders still cannot fully support themselves with their limbs and have unshelled eggs like fish

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6 • Evolutionary timeline:

– Jawless fish – Cambrian Period, 530 MYA – Jawed fish – explosion of fish diversity in Silurian Period (425 MYA) – Terrestrial amphibians – Devonian Period (400 MYA)

• Adaptations of some lobe-finned fish that allowed emergence onto land:

– Limbs with digits – Lungs – A primitive neck

• Fish-like ancestors probably evolved these traits in shallow swamps with stagnant water

– Competition and an abundance of unexploited resources may have drove vertebrates onto land

– Another theory is that early amphibians lived and fed in water but deposited eggs in moist places on land for better survival of eggs and larvae

Coelacanth – modern lobe-finned fish

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7 • The amniotic egg: reptiles, birds, mammals (amniotes)

– Carboniferous Period (320 MYA)

– To this day, amphibian eggs are still very similar to those of fish and must be placed in moist areas to develop; no protective shell

– Seems to have developed to increase protection of terrestrial eggs from microbes

– First, a fibrous shell evolved then, as added protection, a calcerous (calcium) layer was added

– All modern-day reptiles deposit calcium crystals in a fibrous matrix

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8 – Today, most reptile eggs must absorb moisture from the environment to complete development

– It is not clear whether extraembyronic membranes evolved within primitive eggs or female’s oviducts

– Earliest amniotes were a group of labyrinthodonts called anthracosaurs (below)

• Amniotes – extraembryonic membranes

– Do not need water to reproduce, no larval stage

– Chorion, amnion, and allantois provide metabolic support for developing embryo

– Yolk sac provides food

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9 • Adaptive modifications required for terrestrial life:

1. Embryonic development not dependent on standing water

2. Direct development of embryo without a free-living larval stage

3. Skeletal and muscular support to withstand increased force of gravity

4. Feeding – shifts in morphology (shape of jaws) and behavior

5. Modification of integument to withstand friction, abrasion, and evaporation rates

• Amphibians have more cell layers and a keratinized outer layer of skin that fish lack which helps reduce friction and punctures by foreign objects but does not reduce evaporation rates

• Amniotes evolved even more cell layers and more keratin to outer layers to reduce evaporation

• Thicker skin also aided in support of internal organs

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10 • Early reptiles – Carboniferous Period 300 MYA

– During this time, plants were becoming abundant and diverse on land providing a food source

– Until then, vertebrates were primarily carnivorous, as most extant primitive fishes (catfish, lungfish, gar, bowfin) and amphibians are today

– The only terrestrial animal prey available was fast-moving invertebrates (spiders, centipedes, and mites)

– An explosion of reptile species began (adaptive radiation) when they became herbivorous

– Earliest reptiles were cotylosaurs, represented by Hylonomus which still had many amphibian-like traits such as its skull, limbs, and girdle

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11 Therapsida – the earliest mammals Permian Period 250 mya

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Systematics and Taxonomy of Herpetofauna

• Systematics - the scientific study of the kinds and diversity of organisms and any and all relationships among them • The study of biodiversity and its historical (evolutionary) and contemporary patterns and processes, which involves the comparative study of living and fossil species

• In the past, anatomical structures were used to infer relationships but there were problems discerning traits that were homologous (similar in appearance because of common ancestry) or a result of convergent evolution (analogous)

• Convergent evolution has occurred often and is the result of animals with no recent common ancestor that have adapted to similar habitats and lifestyles in different regions of the planet

Aardvark - Africa Giant anteater – South America

3 Species evolved to eat Sloth bear – ants and termites on India different continents

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• One great example is comparing Australian marsupial mammals with North American placental mammals

• Now, DNA is used from living forms to derive relationships so we can more easily look at evolutionary descent

• Taxonomy - the practice and science of classification

– Taxonomies are composed of taxonomic units known as taxa (singular taxon) and are hierarchical in structure

– As you drop from one level to the next, the taxa become more and more exclusive

Examples of convergent evolution of placental mammals and Australian marsupials

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• Early tetrapod evolution

– Early relationships among evolving vertebrates are confusing and several scenarios are presented

– We believe all tetrapods descended from one group of bony fish (Osteichthyes) that were members of the fleshy-finned group (Sarcopterygii: coelacanth, lungfish) rather than ray-finned fish (Actinopterygii: sunfish, snapper, gar)

– By mid-Permian (transition from Paleozoic to Mesozoic Era), amphibians and reptiles had diversified and radiated onto land

• Amniotes were becoming dominant and consisted of more species and individuals than anamniotes

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• The climate where tetrapods were evolving was hot and wet, and dense plant communities were found in valleys but upland plants were beginning to radiate

• The herpetofauna living today represent remnant lineages of very diverse groups that shared some traits of amphibians and/or reptiles

• Living and extinct (fossilized) species are grouped into higher taxa by temporal fenestrae (openings in the skull)

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• In the Triassic Period (early Mesozoic):

– Dominant terrestrial vertebrates were reptiles and synapsids

– Lissamphibians (modern amphibians) first appear in the fossil record although they probably date back to Permian

– Some marine amphibians existed (a rarity)

– The first lissamphibian in the fossil record is Triadobatrachus massinoti, a frog from the lower Triassic found in Madagascar

• Its pelvic girdle and skull are very similar to modern frogs but it had more body vertebrae (14) that were unfused and 6 tail vertebrae

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Higher taxonomy of modern amphibian

• Class Amphibia

– Order Urodela (extant species)/Caudata – Salamanders

• Lizard-like in appearance and most are small (largest is the giant Chinese salamander at 6 ft. and 140 lbs.)

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• Salamanders

– Earliest fossils are from the middle Jurassic found in England

– Fossils have been found in the northern hemisphere around the world and South America is the only southern continent with a significant distribution of species from one family

– It appears they have always been found in forested temperate regions (like much of the Southeast)

– Extant species comprise 3 clades: sirenoids, cryptobranchoids, and salamandroids

– At least 410 species from 13 families worldwide and 28 species in MS from 7 families

– In general, well developed tail, Siren cylindrical elongate body, and a distinct head – Most have well developed limbs but have been reduced in some species

Hellbender

Newt

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Local Families

• Order Caudata – salamanders

– Family Chryptobranchidae: hellbenders/Chryptobranchus – 1 species in MS

– Family Proteidae: mudpuppies and waterdogs/Necturus – 3-4 species in MS

– Family Amphiumidae: amphiumas/Amphiuma – 3 species in MS

– Family Sirenidae: sirens/Siren – 1 species in MS

– Family Ambystomidae: mole salamanders/Ambystoma – 5 species in MS

– Family Salamandridae: newts/Notophthalmus – 1 species in MS

– Family Plethodontidae: lungless salamanders/several genera

• Aneides – climbing salamanders/1 species • Desmognathus – dusky salamanders/2 species • Eurycea – stream salamanders/5 species • Gyrinophilus – spring salamanders/1 species • Hemidactylium – 4-toed salamanders/1 species • Plethodon – woodland salamanders/4 species • Pseudotriton – red salamanders/3 species

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• Order Anura/Salientia (old name) – Frogs

• One of the most diverse groups of vertebrates and account for 88% of amphibian species • Most are found in moist habitat but some have evolved life histories that allow them to live in deserts

•Frogs

– Fossils have been found all over the world reflecting a wide distribution that we still see today

– Abundant in temperate and tropical regions but much more diverse and abundant in the tropics

– Always more diverse and abundant than caecilians and salamanders; found along coasts and on mountains

– About 4,800 species in 33 families occur worldwide on all continents except Antarctica (29 species from 5 families in MS)

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Local Families • Order Anura - frogs and toads

– Family Bufonidae: toads/Bufo (now Anaxyrus for most and Ollotis for gulf coast toad) – 6 species

– Family Pelobatidae: spadefoot toads/Scaphiopus – 1 species

– Family Microhylidae - narrowmouth toads/Gastrophryne – 1 species

– Family Ranidae - true frogs/Rana (now Lithobates) – 9 species

– Family Hylidae - tree frogs, cricket frogs, and chorus frogs/Hyla, Acris, Pseudacris – 15 species

– Order Gymnophiona (extant species)/Apoda – Caecilians

• Several unique traits for underground life • All have a set of small tentacles for sensory reception • Muscular and skeletal elements of the head are modified for rigidity for burrowing • Protective covering over eyes that are very reduced

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• Caecilians

– First fossil is from the early Jurassic from the southwestern U.S.

– Other fossils have been found from Brazil, Bolivia, and Sudan (Africa) indicating a wide historic distribution

– Now they are restricted to tropical and sub-tropical areas around the world

– Currently, we recognize 160 species in 6 families (none in the U.S.)

– In general, small, no legs, wormlike appearance, fossorial

Living Caecilians

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12 Examples of convergent evolution of placental mammals and Australian marsupials 29 30 31 32 33 8/26/2014

• The Mesozoic Era was the Age of Reptiles

– Many marine and terrestrial species including some capable of flight mainly by gliding

– Much like the amphibians, the majority of reptile species and lineages are now extinct

• Class Reptilia

• Order Crocodilia – Crocodilians

• Appeared first in the late Cretaceous and most abundant during the Tertiary when they radiated over most of the temperate and tropical regions of the planet

• 23 species in 3 families found in the tropics and sub-tropics

• 3 extant groups/Superfamilies: gavialoid, alligatoroid, and crocodyloids

• One local species, the American alligator in Family Alligatoridae

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Distribution of Order Crocodilia

Crocodile Alligator

Gharial

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• Order Testudines

– Earliest fossils from the late Triassic and their bony shells left a great fossilized record

– Still found on every continent except Antarctica from coasts to small streams

– Also, found in every ocean and connected sea from Alaska to New Zealand

– 285 species in 18 families

– Two groups/Suborders: pleurodires (side-necked, all southern hemisphere) and cryptodires (hidden-necked)

Distribution of Order Testudines

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Alligator snapping turtle Galapagos tortoise

Leatherback turtle

Softshell turtle

Sideneck turtle

Local Families

• Family Cheloniidae: most sea turtles/4 genera – 4 species

• Family Dermochelyidae: leatherback sea turtle/Dermochelys – 1 species

• Family Chelydridae: snapping turtles/Macroclemys and Chelydra – 2 species, alligator snapping turtle and common snapper

• Family Testudinidae: gopher tortoise/Gopherus – 1 species

• Family Trionychidae - softshell turtles/Apalone – 2 species

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• Family Kinosternidae: mud and musk turtles/Kinosternon and Sternotherus – 5 species

• Family Emydidae: aquatic “pond” turtles and box turtles in 6 genera

– 15 species in MS and a highly variable group including:

• Chrysemys – painted turtles (colorful) • Deirochelys – chicken turtles (very long necks) • Graptemys – map turtles (highly ridged carapace) • Malaclemys – diamondback terrapin (salt marsh turtle) • Pseudemys – cooters (large river turtles) • Trachemys – pond sliders (most common turtle) • Terrapene – box turtles (common land turtle)

• Order Sphenodontia/Rhyncocephalia (old name)

– Family Spenodontidae – Tuataras

• Most abundant from Triassic to Cretaceous but never very abundant or diverse

• Differ from other lizards by some archaic traits: gastralia (stomach ribs), several skull characteristics including dentition and location of temporal fenestrae

• Now, restricted to 2 species from 1 family in New Zealand only on smaller islands (none in New World)

• Does not compete well with modern lizards and almost wiped out by the introduction of mammals

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• Order Squamata

– Suborder Sauria /Lacertilia (old name) – Lizards

• Earliest fossils are from the Jurassic and the fossil record shows immense radiation in the Cretaceous

• Still a very diverse group (the most diverse of reptiles) with 4,450 species from 21 families

• Found on every continent except Antarctica from tropical, temperate, and arid regions

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Distribution of all Order Squamata

Local Families

• Family Anguidae: glass and alligator lizards/Ophisaurus – 3 species

• Family Polychrotidae: 372 species of anoles, all in the New World – 2 species of Anolis in MS

• Family Scincidae: skinks/Eumeces and Scincella – 6 species

Glass lizard

Broadhead skink

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• Family Phrynosomatidae: spiny lizards/Sceloporus – 1 species (eastern fence lizard)

• Family Teiidae: whiptails/Cnemidophorus – 1 species (6-lined racerunner)

• Family Gekkonidae: geckos/Hemidactylus – 1 species in MS (Mediterranean gecko)

Mediterranean gecko

Eastern fence lizard

• Suborder Serpentes (extant species)/Ophidia – Snakes

– First fossil is from the early Cretaceous and from there they have increased in diversity

– Found on all continents except Antarctica from coastal areas to mountains and from tropics to temperate regions

– 2,900 species in 17 families

– Snakes evolved from lizards and are grouped in the same clade

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• They share almost all important anatomical and physiological traits except for:

1. The presence of limbs (though remnant girdles and limb buds are present in some older groups)

2. Disarticulate jaw (lizards can’t)

3. Absence of eyelids and external ear (below)

Local Families

• Family Elapidae: coral snake/Micrurus – 1 species in MS but many worldwide (includes cobras, mambas, boomslang, sea snakes)

• Family Viperidae: pit vipers

• Agkistrodon - copperhead and cottonmouth (moccasin) • Crotalus and Sistrurus – rattlesnakes

• Family Colubridae: highly variable family with 19 genera and 35 species (not including sub-species) • Carphophis – 2 species of wormsnakes in MS • Diadophis – 1 species of ring-necked snake • Rhadinea – 1 species of littersnake

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– Cemophora – scarletsnakes – Coluber – racers – Drymarchon – indigo snakes – Elaphe (now Pantherophsis) – ratsnakes – Lampropeltis – kingsnakes – Masticophis – whipsnakes – Opheodrys – greensnakes – Pituophis – pinesnakes – Tantilla – black-headed snakes – Nerodia – North American watersnakes – Regina – crayfish snakes – Storeria – North American brownsnakes

– Thamnophis – North American gartersnakes – Virginia – North American earthsnakes – Farancia – mudsnakes (1 species) – Heterodon – hognosed snakes (1 species)

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• Suborder Amphisbaenia – worm lizards

– Mostly in Africa and South America (some in FL, none in MS)

– Wormlike in appearance and most are < 6 inches long

– All are fossorial so we don’t know much about them

– A bit like snakes but some differences:

1. Have only the right lung (snakes have left lung)

2. Most of the skull is a solid bone with a single median (centered) tooth in the upper jaw

3. A few have reduced forelimbs but all have remnants of pelvic and pectoral girdle (rare in snakes)

4. Some species can shed their tails to distract predators (no snakes can)

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12 Amphibian Embryonic Development • Eggs

– Tetrapod zygotes (developing embryo) must have some protection from microorganisms, physiological challenges (dehydration), and abiotic physical threats (puncture, abrasion)

– A protective layer of mucoprotiens and mucopolysaccharides are deposited around the ova before external depostion and these form the strings and balls of eggs seen in pools and streams

– Sperm can penetrate the defensive layers either in the cloaca (internal fertilization) or just as they are shed

Spotted salamander eggs and larvae with symbiotic green algae providing oxygen

Poison dart frog (Mantella) with Wood frog eggs (Rana) Toad eggs (Bufo) eggs in a stumphole

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1 • Larvae

– Most free-living larvae feed but some depend on yolk reserves (direct developers have a brief larval stage after hatching)

– In general, caecilian and salamander larvae resemble adults and anuran larvae do not and must undergo major reorganization during metamorphosis (transition from larval to adult stage)

– Tadpoles vary greatly in morphology depending on the habitat they’re adapted to with 18 ecomorphological guilds identified (Ron Altig did most of this work)

• All have a large coiled intestine for absorbing nutrients from vegetation (they’re carnivorous as adults)

• Most have a fleshy disc encircling their mouth that may be found ventrally (to anchor in moving water and graze on rocks) or dorsally (to graze on surface film in stagnant water)

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2 Aquatic/pond larval types: mudpuppy, spotted salamander, newt

Direct development: Plethodon sp. Aquatic/stream larvae: Eurycea

Anura larvae: bullfrog, spring peeper

Adult Amphibian Biology • General morphology

– Mostly bony skeleton – No claws or true nails – Smooth, moist, glandular skin (no scales) – Gas exchange by lungs, gills, or skin and not all have lungs

• Integument

– Permeable to water and gases

• Water can be absorbed from soil or other substrates • Up to 70% of water absorbtion occurs on a ventral, pelvic region called the “seat patch” • Minerals can also be absorbed

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3 – Consists of 2 parts

1. Epidermis – outer layer consisting of:

– Stratum corneum – outer layer of dead keratinized cells that aids in retaining moisture

– Middle transitional layer

– Stratum germinativum – gives rise to epidermal cells and has mucous and granular (poison) glands

2. Dermis – inner layer that gives rise to glandular cells

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4 – Molting – shedding of keratinized tissue

• Occurs in all species, aquatic and terrestrial

• Happens less frequently in adults and related to food intake

– Granular glands – produce noxious (irritating) or toxic (life- threatening) secretions

• The newts Notopthalmus and Taricha produce neurotoxic tetrodotoxin that stops involuntary muscle action (breathing, heart) and is the same toxin found in pufferfish

Taricha sp.

– African clawed frogs produce antibiotic peptides that can kill bacteria, fungi, micro-parasites, and some viruses

– Poison arrow frogs (Dendrobates, Phyllobates) have enough toxin in skin to kill several humans

• Causes muscles to stay in a contracted state and cardiac failure

• Those in captivity stop producing toxin so something in their natural diet supplies them with the toxin

– Other modifications • Skin folds for extra surface area for gas exchange • Toe pads for climbing • Toe webbing for improved swimming

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5 • Chromatophores include:

– Melanophores (black) – Iridophores (iridescence) – Xanthophores (color)

• Skeletal system

– More ossified than fish with loss and fusion of elements and much modification of appendicular (limbs) skeleton for terrestrial locomotion

– First true sternum appears but no ribs attach to it so mainly a site for muscle attachment

– Vertebrae: salamanders up to 100, caecilians up to 285, and frogs about 8

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6 • Most have 4 legs but there are exceptions

– Caecilians have lost girdle and limbs

– Amphiuma has girdles and limbs but they’re vestigial (no longer useful)

• Frogs have an exceptionally fused skeleton for hopping and absorbing shock

• As you go up the evolutionary amphibian tree, bones are lost or fused

• Muscular system

– Salamander (especially aquatic) musculature similar to fishes

• Metamerism (myomere divisions) are still very evident and abundant • Larval anurans and caecilians retain myomeres • Locomotion is still primarily from trunk muscles and limbs not that important

– As vertebrates moved to land, locomotion becomes primarily from limbs

• Segmentation becomes obscured by sprawling appendicular muscles • Terrestrial salamanders still have an undulatory movement

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7 • Cardivascular system

– Heart develops internal septum to separate oxygenated blood from deoxygenated blood

• Most have 3 chambered heart, 2 atria and 1 ventricle, and the ventricle has begun to separate in some species

• 1 atrium receives body blood (deoxygenated) and the other pulmonary blood (oxygenated)

• Some blood travels from the heart via cutaneous arteries to the skin for cutaneous (skin) respiration

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8 Typical 4-chambered mammal heart

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9 – All amphibians use cutaneous respiration to some degree and lungless salamanders (Plethodontidae: 70% of living salamanders) are almost entirely dependent on it

• Respiratory system

– Air travels through external nostrils directly into the oral cavity (amphibians do not have a secondary palate as we do)

• Air goes from trachea to the lungs

– They are the most primitive vertebrates to have a larynx (voice box) at the end of the trachea with vocal cords

– Most male frogs have vocal sacs to gather air and a species-specific call

– Air is forceably pumped to the lungs

• After air enters the oral cavity, the nostrils are closed and the floor of the cavity is raised forcing air into the lungs

• More advanced vertebrates use rib muscles and a diaphragm to pump air

– Larval salamanders have exposed external gills and tadpoles (larval frogs) have gills but they’re enclosed and water reaches them via a spiracle (a hole on the side of the head)

• Some aquatic salamanders lose their gills and develop lungs (hellbenders and amphiumas)

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10 • Some retain gills (mudpuppies and sirens) and have lungs

– This is neoteny or retention of larval traits – At one time their ancestors developed into land forms then later reverted to an aquatic life

– Frog lungs may be lined with respiratory pockets (alveoli) to increase surface area for gas exchange and they rely more on oxygen from lungs than other amphibians

• Digestive system

– Frog tongues are attached at the front of the lower jaw and are specialized for obtaining food with specialized cells that keep a sticky coating on the end

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11 – Teeth are all shaped alike (homodont dentition) and attached on the inner side of the jawbone (pleurodont dentition)

• Teeth can also be found on the palate • They are for grasping and holding food, not for chewing

– Pathway for food:

• Mouth – not very specialized in most cases with frogs having the most unique (we’ll discuss feeding later) • Stomach – for holding and digesting and not specialized • Intestines – of variable lengths; longer for herbivorous species and shorter for carnivorous species • Cloaca – one opening that receives contents of digestive, urinary, and reproductive tracts

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12 • Nervous system

– A pineal organ remains in the brain but not very well developed

• In ancient vertebrates (lamprey), this organ was very important for daily and annual regulation of activities

• Probably still used for photoreception in some species

– Optic lobes are well developed but the cerebellum is small (probably because locomotion is relatively simple)

• Sense organs

– Neuromast organs (vibrations) – larval and aquatic amphibians have later-line and cephalic (head) canals

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13 – Ear

• 3 divisions:

1. Outer – tympanum for airborne vibrations 2. Middle – transmit vibrations from tympanum to inner ear via the columella 3. Inner ear (3 semicircular canals, each in a different plane)

• All can hear but frogs have the best hearing

– Eyes – several advances over fishes

• Salamanders have good color vision and frogs have some

• In frogs, a transparent membrane (nictitating membrane) protects the eye when the eyelid isn’t shut

• Some cave-dwelling salamanders have vestigial eyes

Olm (Proteus anguinus) lives in underground caves in Europe

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14 • Nose – some advances over fishes

– As air enters it passes over olfactory epithelium (smelling skin)

– First group with a vomeronasal gland (Jacobson’s organ) which gives better reception of olfactory signals, especially pheromones

– Plethodontid salamanders have nasolabial grooves for extra pheromone reception

– Caecilians have a tentacle on each side of the head for under ground chemoreception (we’ll discuss it more later when we get to communication)

– Taste – gustatory cells are found on floor of mouth, jaws, and palate but none on the body as in fishes

• Urogenital system

– Kidneys are more advanced than fishes and forms urine in terrestrial amphibians (ammonia is formed in fishes)

– Bladders are present in all to store urine and helps in water and ion exchange

– Females have well developed oviducts with cells that secrete jelly envelopes onto eggs

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15 – Female salamanders with internal fertilization have a sperm storage sac (spermatheca) and eggs are fertilized as they pass

– Males have duct, vas deferens, which transports sperm to cloaca

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16 62 63 64 Reptile Biology • Integument

– For water retention and protection

• Much better at reducing water loss than amphibians (permits them to live in hot, dry climates) • Amphibians use skin glands to produce protective substances but reptiles rely on armor-like skin for protection – Turtle scales form from the epidermis and may be >6 layers thick

• The shell is formed by dermal bony plates with a thin covering of hard, keratinized scales (top is carapace and bottom is plastron)

• The thin scales are sloughed periodically but the shell grows with the turtle

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1 – Lizard and snake scales also come from the epidermis and it consists of the traditional 3 layers as we saw in amphibians

• Scales project backwards and overlap to form a solid sheet

• Number and arrangement of scales are used extensively to identify species

• Most shed in one piece (ecdysis)

• Many snakes use broad belly scales, called scutes, for locomotion

• Most lizards have claws that are shed periodically and regrow, whereas bird and mammal claws continually grow and are worn down

– Dermis has chromatophores similar to amphibians but not as abundant in most

• For:

1. Protection (camo and warning patterns)

2. Social status

3. Sex recognition

4. Thermoregulation (dark vs. light)

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2 • Skeletal system

– Turtles developed a secondary palate in the skull

• Allows food to be processed (tearing and crushing) without affecting breathing

• Most other reptiles (lizards and snakes) have no need for this since they swallow their prey whole

– Vertebrae are more specialized in reptiles than amphibians

• Lizard vertebrae are differentiated into thoracic (chest), lumbar (back), and caudal (tail)

• Snake vertebrae have pre (before vent) and post caudal (after vent) section

• Many lizards and a few snakes can release their tails to avoid capture (caudal autotomy)

Skink tail lost to distract predator

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3 • Appendicular skeleton

– Diverse locomotion and limb arrangements

– Limbs are set vertically compared to amphibians and weight is better supported this way and legs serve as shock absorbers

– Most snakes and some lizards (glass lizards) lack one

– Boas and pythons have vestigial pelvic girdles and visible spurs where there were once legs

Burmese python

• Muscular system

– Much less metamerism than amphibians (muscles now arranged in bundles)

– Appendicular muscles much heavier so limbs can fully support body

– First group of vertebrates with integumentary muscles capable of moving the skin

• Cardiovascular system

– Reptiles are completely dependent on the lungs to re- oxygenate the blood (there are rare exceptions) so pulmonary circulation must be more efficient

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4 – Turtles, snakes, and lizards have a 3 chambered heart with the ventricle only partially divided (atrium is fully divided)

– Crocodilians have a 4 chambered heart with the ventricle fully divided

• Only one lung is functional in snakes and legless lizards so corresponding vessels become vestigial during development

• Respiratory system – Snakes have a tube (glottis) they can extend from the floor of the mouth so they can breathe while swallowing large prey – Most reptiles are voiceless but some lizards and turtles do have vocal cords

• Geckos “bark” and some anoles can make squeaking noises

– Lungs are better developed than amphibian lungs

• Turtles and squamate lungs have many sub-chambers (faveoli) to increase gas exchange surface

• Tuataras have simple sacs for lungs (they aren’t very active due to oxygen consumption restraints)

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5 Histological sites of O2-CO2 exchange surfaces in (A) alveolar (mammalian) and (B) modified septate (avian) lungs. Whole-lung cross (C) and longitudinal (D) sections of unmodified sauropsid (lizard) septate lungs (Varanus). Mammalian and avian lungs consist of millions of these individual respiratory units [(A) and (B)]. Respiratory exchange in unmodified sauropsid lungs [(C) and (D)] takes place on septal surfaces.

Percentage of cutaneous gas exchange in various herpetiles

White bar = O2 uptake Black bar = CO2 excretion

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6 – Some reptiles use the floor of the mouth to force-pump air but some are able to actively suck air into the lungs by movements of the ribs by the intercostal muscles – Some aquatic turtles can obtain oxygen from the throat, cloacal bladder, and/or skin while submerged in water – Sea snakes can obtain oxygen thru their skin while submerged

• Digestive system – Jaws are covered by immovable thickened lips – Turtle jaws are covered with a shell of keratin that forms a beak

– All reptiles except turtles have teeth • Most have homodont dentition but some lizards and crocodilians have heterodont dentition with specialized incisors, canines, and molars

• Most lizards and snakes have acrodont (teeth attached to the rim of the jaw) or pleurodont (teeth attached to the inner side of the jaw) dentition

• Crocodilians have teeth rooted in sockets (thecodont)

• Most reptiles are polyphyodont (replace teeth continually) but the tuatara are monophyodont (one set of teeth for life)

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7 Gila monster Only one genus of venomous lizards in the world, Heloderma, with 2 species, the Gila monster and the Mexican beaded lizard, with venom that flows upward along grooves in bottom jaw teeth

• Snake and lizard venom – formed from modified salivary glands

– Some species in the family Colubridae have rear fangs on the upper jaw with simple grooves that deliver mild venom

• Most are no danger to humans (SE crowned snake, hognose snake)

• The boomslang of Africa is a rare exception

SE crowned snake Tantilla coronata

About 600-700 of almost 3,000 snake species are venomous to some degree

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8 – Snakes in the family Elapidae have fixed fangs on the front of the upper jaw that are grooved or hollow

• Venom is primarily neurotoxic and many are very lethal (cobras, coral snakes, sea snakes, most of Australia’s snakes)

• Antivenin (antivenom) is usually very effective and residual problems are minimal

The inland taipan or fierce snake of Australia may be the most lethal terrestrial snake in the world based on L.D. 50 tests on mice. Some sea snakes have the most potent venom.

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9 – Pit vipers and vipers of the families Crotalidae and Viperidae have the most specialized fangs • Long, hollow, hinged fangs on the front, upper jaw swing outward when the mouth opens for a very efficient delivery system • Venom is primarily hemotoxic and many are very lethal • Rattlesnakes, cottonmouths, saw-scaled vipers (kill as many as 50,000 people/year in Africa and Asia), gaboon viper (fangs can be 2” in length) • Antivenin can be effective but necrosis usually remains

Asp viper – no pit

– Snakes and some lizards have specialized forked tongues for “smelling” the environment

• The tongue collects molecules and returns to the roof of the mouth to the vomeronasal (Jacobson’s) organ to deliver information

– The stomach, small, and large intestines are distinct

• Some herbivorous species (some lizards and turtles) have a cecum along the intestine that stores bacteria to digest plant material – All snakes except one species of sea snake that feeds on coral algea are carnivorous • Most reptiles have a partially divided cloaca, a vent, that keeps waste and reproductive elements separate

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10 • Nervous system

– The cerebrum and cerebellum of most reptiles are considerably more advanced than amphibians

• The hypothalamus acts as a thermostat and controls bodily temperature by controlling behavior (basking poikilothermy)

• The first group of vertebrates with distinct auditory lobes

• Other sense organs

– Skin receptors

• No lateral-line systems exist

• Many pressure, tension, pain, and temperature receptors are found in the skin

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11 • Heat sensing pits, loreal pits, are found on the head of pit vipers, boas, and pythons and can sense a change of 0.003 C and are able to hunt in the dark

– Ear • Snakes have reduced hearing capability

– They lack a tympanum and middle ear but can detect airborne sounds to some degree via the jaw

• Most other reptiles have a visible tympanum and can detect airborne sounds but not as well as birds and mammals (they can detect ground vibrations better than birds and mammals)

Glass lizard Water snake

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12 – Eyes

• In snakes and some lizards, eyelids are sealed shut and are transparent

• Turtles and some lizards have a second eyelid, nictitating membrane, that cleans and lubricates the eye when other eyelids are open (useful in aquatic environments)

• Many reptiles have lacrimal glands (tears) to keep eyes moist and clean (very important in sea turtles where they help in osmoregulation by excreting salt)

• Many diurnal (active during the day) snakes and lizards only have cones (color detecting cells) in the eyes and cannot see in low light conditions at all

• Most other reptiles have cones and rods (light gathering cells) and see much like humans

– Taste

• Poorer than in fishes and amphibians but can still play a role in recognition of prey, enemies, and mates

• Gustatory cells are usually found in the pharynx but few, if any, on the tongue

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13 Urogenital system • Excretion of nitrogenous waste – Reptiles are the first vertebrates to have advanced, true kidneys that are designed for a fully terrestrial life

– The metabolism of proteins for maintenance of tissues produces nitrogenous products that are toxic if they accumulate – Vertebrates excrete nitrogenous waste as ammonia, urea, or uric acid

• Aquatic vertebrates (fish, some amphibians and reptiles) aren’t concerned with water conservation so they excrete the simplest type of waste NH3(ammonia), which is water soluble and very toxic

• While many amphibians produce almost pure ammonia, aquatic reptiles excrete an ammonia/urea mixture (turtles, alligators)

– To conserve water, mammals and some reptiles excrete urea, a

more complex molecule (NH2X2)

• Requires less water to expel compared with ammonia

• Not as toxic and can be stored (bladder) or accumulate in the bloodstream for short periods

• Reptiles may produce a mixture of urea and uric acid depending on species

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14 – Birds need to be as light as possible so they excrete uric acid (NHx4) which can be stored as a semi-solid suspension that requires very little water to expel

• Birds and reptiles need only 0.5-1.0 mm of water to excrete 370 ml of uric acid

• Mammals need 20 mm of water to excrete the same amount of nitrogenous waste or 20-40 X more water

• Reptiles excrete uric acid to conserve water in arid environments

Ammonia Urea

Uric acid

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15 – Salt excreting glands are present in marine species

1. Marine turtles have the lacrimal gland of the eye 2. Marine iguanas and some desert lizards have nasal organs 3. Sea snakes have a gland in the palate of the mouth

• Reproduction

– Oviducts leading from ovaries to the cloaca have shell glands that coat eggs with a shell as they go down the duct

– Some female snakes and lizards have a spermathecae for sperm storage

– Male snakes and lizards have paired copulatory organs, hemipenis, that have no erectile tissue but are turned inside out when needed

– Male turtles and crocodilians have an unpaired penis with some erectile tissue

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16 REPTILES YEARS Giant Tortoise 152 Box Turtle 123 Alligator 68 Snapping Turtle 57 Cobra 28 Cottonmouth 21

AMPHIBIANS YEARS Giant Salamander 55 Toad 36 Bullfrog 30 Mud Puppy 23 Green Frog 10 Newt 7

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Egg Types and Development

• 3 types of ova – based on amount of yolk

1. Isolecithal – small amount of yolk evenly distributed

• Mammal ova contain little yolk because the embryo will get nutrition from the mother

2. Mesolecithal – moderate yolk

• Amphibian ova contain more yolk to allow development of the embryo to the larval stage where it must hatch and start gathering nutrition from the environment

• Most direct-developing amphibian ova approach macrolecithal size

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3. Macrolecithal – heavily yolked

• Reptile ova must begin with enough nutrition in the egg for development to the adult stage

• Development in an egg

– 3 things affect embryonic development in an egg: temperature, water availability, and gas exchange

– In general, amphibian eggs are laid in moister environments than reptile eggs because developing larvae are aquatic and can exchange gas while inundated

– Reptile embryos will suffocate if immersed because inadequate gases are transferred for development

– Reptiles must select egg-laying sites that will provide the correct supply of moisture

• 3 types of birth

1. Oviparous – eggs are deposited outside of body and embryo gets nutrition from yolk

– Most reptiles – Nearly all amphibians – Monotreme mammals – All birds

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2. Viviparous – embryos develop within female (in most cases) and get nutrition from female and yolk (live-birth)

– Nearly all mammals (nutrition supplied through placenta)

– Some caecilians

• Truly viviparous – eggs hatch within female and larvae feed on transformed oviduct lining

• Intermediate viviparous – eggs are deposited outside of body and larvae feed on transformed outer skin of brooding female

– Probably a step toward true vivipary

3. Ovaviviparous – eggs are kept within female oviduct and they hatch then exit female for live-birth (all nutrition is taken from the yolk and none from the female)

– Some reptiles (some skinks, vipers) – Some frogs – Some caecilians

• Mode of birth will dictate how many offspring are produced in one reproductive cycle

– Viviparous species have fewest offspring because they emerge well-developed and are somewhat able to fend for themselves (independence from parents is highly variable)

– Caecilians have about 6-8 young

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– Ovoviviparous species tend to have a few more offspring on average

• Vipers may have up to 12 and skinks 8 in a litter

– Oviparous species tend to lay numerous eggs but is dependent on species

• Direct developing frogs may lay scores of eggs while some with free-living larvae may produce several thousand

Amphibian Reproduction and Life Histories

• All reproduction in vertebrates begins with external or internal fertilization

– External – ovum and sperm fuse outside the female body

– Internal – ovum and sperm fuse, usually, in female oviduct

– Amphibians display the most diverse reproductive modes of terrestrial vertebrates because they evolved first and “experimented” reproductively as they radiated onto land

– Comparatively, bird and mammal reproduction is uniform across taxa

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• The most primitive form of animal reproduction is synchronous shedding of eggs and sperm into water

– Most aquatic invertebrates (sponges, crustaceans, mollusks) and fishes rely on this method – No tetrapod uses this unreliable mode

• In even the most primitive species, courtship takes place which provides at least 2 advantages:

1. Gametes are brought close together

2. Courtship ensures both sexes have mature gametes

• External fertilization occurs in most frogs and some salamanders (Cryptobranchidae, Hynobiidae)

– In most frogs, males grasps females in front of the hindlimbs (inguinal) or behind the forelimbs (axillary) so that their cloacae are adjacent, but amplexus is highly variable

– In salamanders, males follow females and deposit sperm on eggs as they pass over

• To better ensure fertilization many amphibians rely on internal fertilization:

– Few frogs: Ascaphus (tailed frog of the Rocky Mts. and 6 other species)

– All salamandroid (most extant species) salamanders

– All caecilians

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• Frogs with internal fertilization use either cloacal apposition (Fig. 4.6, center position) or an intromittent organ (Ascaphus)

• Caecilians have an intromittent organ called a phallodeum that deposits sperm into the female cloaca

• Male salamanders produce a spermatophore (sperm packet) on a gelatinous pedestal that is deposited on the ground for the female to pick up

– Males must entice females with displays and pheromones to walk over the packet and draw it into her cloaca

– Females take in spermatophores and store them in the spermatheca in the roof of the cloaca then sperm is squeezed out by muscular contractions as eggs are deposited

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Ascaphus truei Salamander spermatophore

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• 3 types of fetal nutrition depending on where they obtain nutrients (all are seen in amphibians):

– Lecithotrophy – all nutrition comes from the yolk – Matrotrophy – at least some nutrients from mother – Patrotrophy – at least some nutrients from the father

• Caecilians

– All species have phallodeum and internal fertilization – >50% are viviparous (matrotrophy/histophagy), rest are oviparous – Oviparous species have direct development or aquatic larvae

• Salamanders

– External fertilization in primitive groups, Hynobiidae, Cryptobranchidae, and Sirenidae; all others internal using spermatophores (no intromittent organs)

– For Salamandroidea:

a) Eggs and larvae aquatic: Eurycea (two- and three-lined salamanders)

b) Eggs terrestrial and larvae aquatic or terrestrial: Marbled salamander has terrestrial eggs and aquatic larvae and must rely on filling of ephemeral forest pools

c) Eggs terrestrial with direct development: most of Plethodontidae

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Hynobiidae

Cryptobranchus Siren

• 4 species are viviparous, all Salamandridae from mountainous regions of Europe

Salamandra atra Salamandra salamandra

Mertensiella sp.

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• Anurans

– Greatest diversity in reproductive modes of all terrestrial vertebrates (29 categories) based on:

• Egg placement • Clutch structure • Breeding site • Larval development site • Parental care, if any

– Eggs are placed in 3 locations: aquatic, terrestrial, or retained in body

• Aquatic eggs - aquatic eggs with aquatic larvae is the ancestral condition (many species)

– Some tropical hylids deposit eggs in water-holding structures (bamboo nodes, bromeliads, stumpholes)

• Male leaves after fertilization but female returns to feed tadpoles unfertilized eggs to eat (oophagy)

– Australian gastric brooding frog (Rheobatrachus silus) females deposit aquatic eggs, swallow them, young emerge several months later fully developed

• We think young produce a chemical that inhibits production of gastric juices

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– Some tropical frogs construct foam floating nests from cloacal secretions and tadpoles emerge later

– Pipa are aquatic species and males press eggs into the dorsum of females that later emerge as tadpoles or froglets • Terrestrial eggs

– All Dendrobatidae (poison dart frogs) have small clutches on land

• They court on land and deposit eggs in the leaf litter on the forest floor

• Males may attend eggs, wait until they hatch, gather tadpoles on his back and take them to water

Rheobatrachus silus Aquatic foam nest

Pipa pipa (Suriname toad)

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• A few species have nest-loving tadpoles (nidicolous) that do not feed but stay in nest until metamorphosis

– One Australian frog (Assa darlingtoni) female guards egg mass for about 10 days until tadpoles hatch

• Male gathers tadpoles in leg pouches and carry them for 2 months when they hatch as froglets

• Possible patrotrophy but not well documented

– Rhinoderma in Argentina have males that carry tadpoles in pouches on the back or, in one species, in vocal sacs

• Some evidence of patrotrophy has been found

Rhinoderma with froglet

Poison dart frog with tadpoles

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– Most Eleutherodactylus (mostly New World tropics, >650 species) lay egg clutches among vegetation and males guard eggs until they hatch as froglets

• Males travel to pools or streams, absorb water into skin on the belly, and return to moisten developing larvae – Some arboreal frogs in Hylidae and Centrolenidae have arboreal clutches deposited under leaves and branches and after hatching, tadpoles fall into water below

Arboreal foam nests

• Retention of eggs in female oviduct – Only 5 species undergo internal development – Eleutherodactylus jasperi in Puerto Rico has lecithotrophic embryos that emerge as froglets – The other 4 species are in Bufonidae and are found in Africa

Eleutherodactylus coqui male with eggs Centrolenidae (glass frogs) with egg clutch

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13 Asexual Reproduction in Herpetofauna

• A small portion of reptiles and amphibians reproduce asexually

• This can occur via 3 pathways:

– Hybridogenesis – all hybrid populations from 2 parental species

• Females resulting from first hybrid mating continue to produce clones when mating with one of the original species

• The male’s DNA is lost during gametogenesis and the female’s DNA is duplicated resulting in a diploid animal

Hybridogenesis

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1 – Gynogenesis – activation of development by spermatozoon penetration of an ovum without fusion of pronuclei (DNA of parents do not mix)

• Similar to hybridogenesis, involves mating of at least 2 closely related species resulting in diploid or polyploid offspring

• Some salamander species complexes (Ambystoma) produce a wide array of genome combinations involving up to 4 species

• Offspring arise by several types of egg activation and development including gynogenesis

– Parthenogenesis – ovum begins development in the absence of spermatozoon and all female populations result

• Occurs in about 30 species of squamates, mostly lizards (Cnemidophorus, Lacerta)

• This results from hybridization and female offspring begin producing eggs that develop into clones

• It’s not clear what causes eggs to stimulate gametogenesis but pseudocopulation and courtship (between female clones) has been observed in some species

• Unlike the 2 other types of asexual reproduction, these populations contain all clones of one genome

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2 Reptile Reproduction and Life Histories

• All crocodilians, turtles, and tuatara lay eggs

• About 20% of snakes and 20% of lizards are live-bearers with a wide variety of levels of matrotrophy (or lack of)

• Viviparity is much more common in reptiles than amphibians and in some reptiles a placenta nourishes embryos

– The evolutionary transition from oviparity to viviparity included retention of eggs for longer periods of time until eventually no egg shell developed in some species

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3 – In some species (colubrid snake Virginia striatula), embryos are facultative matrotrophs

• They may be nourished from yolk only (lecithotrophic) or they may receive some nutrients (mostly calcium) from the oviduct as the yolk sac is pressed against it

– Once this relationship is established, other nutrients may be transferred across embryonic membranes and the maternal- fetal connections become more complex

– One evolutionary advantage is that females can spread their nutritional commitment to offspring over time (instead of producing eggs with large yolks in a short period of time for lecithotrophic embryos)

– One South American skink genus (Mabuya) has developed a complex placenta similar to true mammals

• This is the first good example we have since the mammals of the Mesozoic Era (250-300 MYA) of the transition from ovipary to true placentotrophy (fetus nourished by placenta)

Several species of Mabuya

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4 • Parental care – any form of post-ovipositional parental behavior that increases the survival of offspring at some expense to the parent

– Includes 6 levels of care ranging from egg attendance to guarding young

1. Nest or egg attendance: crocodilians, some turtles, and many squamates

• Some skinks (Eumeces) and crocodiles regulate egg-water exchange by moving eggs or expanding the nest cavity to expose them to air and prevent them from drowning

• Other advantages include deterring fungal infections and keeping eggs hidden

2. Nest or egg guarding: crocodiles and some squamates

• Female Iguana iguana, Eumeces, cobras, and crocodiles will defend nests from predators and/or conspecifics looking for a place to nest

3. Hatchling transport: female crocodiles carry young to water in their mouth

4. Egg brooding: known only in oviparous boids (pythons)

• Females coil around eggs and shiver which produces heat and causes embryos to develop faster

• In some species, it’s facultative and is triggered by low temperatures and in some it’s obligatory

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5 5. Feeding young: no reptiles; among amphibians, only frogs that provide eggs to tadpoles in special microhabitats (stumpholes, bromeliads)

6. Guarding or attending young: some viviparous squamates and most crocodilians

• Some squamates assist young as they emerge from placental membranes

• Most crocodilians assist in breaking egg shells as hatching young call from inside and transport them to water

• Hatchlings remain in the area with females and emit a stress call that will bring her to their defense

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6 • Most oviparous reptiles construct nests in moist sites (soil, logs, humus, under rocks) because most eggs need some water for development

– Crocodilians construct above-ground nests to protect from flooding

– Most turtles dig nests and cover eggs after deposition

• At least one species (long-necked turtle of Australia, Chelodina rugosa) lays eggs underwater in the sand and development is stopped until floodwaters recede

– Many snakes and lizards and some turtles deposit eggs in termite nests

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7 • For reptiles, mortality is greatest in the egg stage and nest site selection is very important

• Individuals of a species that continually select poor sites will not supply many offspring to the next generation with similar traits

• Sex determination

– Among herpetofauna, sex is determined by genetics or incubation temperature

– All amphibians are heterogametic

– If determined by genetics, most species display heteromorphic gametes in the male (XX/XY) or female (ZZ/ZW)

• A few have gametes that are homomorphic yet sex is determined by genetics (we just can’t distinguish which gamete is male or female by form)

– For reptiles with temperature-dependent sex determination (TSD) the temperature range over which sex is determined is small, sometimes only 2°C between getting all males or females

• Males result from higher temperatures in most crocodilians and lizards

• Females result from higher temperatures in most turtles

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8 • In a few crocs, turtles, and lizards, females develop at high and low temperatures and males intermediate

• The physiological mechanism for TSD involves enzymes that are temperature sensitive

– Aromatase is produced in developing females and 5 alpha-reductase in males

– These enzymes regulate whether dihydrotestosterone or estradiol is produced in abundance

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Physiology: Water and Ions

• Water and ion balance must be maintained for normal cellular activities to occur

– Osmoregulation challenges are different for herpetofauna species depending on what medium they live in

– Osmoregulation - the active regulation of the osmotic pressure of an organism’s fluids to maintain the homeostasis of the organism's water content (it keeps the organism's fluids from becoming too dilute or too concentrated with ions such as sodium and potassium)

– Water loss and ion gain are problems for saltwater species

– Water loss resulting in more concentrated ions is a problem for terrestrial species

– Water gain and ion loss are problems for freshwater species

• Because of differences in skin structure between reptiles and amphibians, they deal with water and ion loss through different pathways

• In freshwater, herpetofauna are hyperosmotic, ion concentration of the body is greater than surroundings

– Permeability of the skin can be decreased

– Urinary output can be increased

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• In saltwater, animals are hypoosmotic

– Permeability of the skin can be decreased

– Urinary output can be decreased but this may lead to toxic levels of nitrogenous wastes and kidneys must assist in regulation of ions

• Terrestrial herpetofauna face a similar situation as marine species but water is lost by evaporation rather than osmosis and kidneys play a big role

• In amphibians, most moisture is absorbed through the skin

– Most terrestrial amphibians have highly vascularized patches of skin somewhere on the body that absorb water

• Amphibian skin is either smooth or granular and it’s the granular skin that absorbs water best

• Aquatic amphibians have smooth skin because water surrounds them

– Terrestrial anurans have patches of granular skin on their thighs (pelvic patch) that absorb water from the soil and 70-80% of necessary water is obtained this way

– Costal grooves of terrestrial salamanders pull water from the soil to their back by capillary action

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• Most reptiles gain almost no water through skin and must drink water, sometimes in strange ways

– Some desert lizards (Coleonyx variegatus) enter cool burrows and drink water from their back as it condenses

– Many South African tortoises collect water along the edge of their carapace and stand so it runs down to their mouth

Coleonyx variegatus Geochelone sulcata Western banded gecko African desert tortoise

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– One desert iguana (Dipsosaurus dorsalis, below) can gain up to 12% of its water through metabolic activity but it’s not enough to account for what is evaporated

• Terrestrial reptiles and amphibians osmoregulate by behavior

– They adjust activities by day and season

– Amphibians must reduce water loss by behavior and with few exceptions, their skin does nothing at all to prevent evaporation

– Some exceptions:

• Some tropical treefrogs can reduce evaporation significantly by a combination of behavior and chemical secretions

1. Some Phyllomedusa (South American hylids) excrete waxy esters and smear it over their body

– This works well up to 35° C when it melts, but the only time of the year when temperatures reach that level is during the rainy season

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Waxy monkey tree frog (Phyllomedusa sp.)

2. High temperatures are the main cause of water loss for South African waterproofed frogs (Chiromantis and Hyperolius) and they’re able to reflect most light by accumulating iridophores in >1 layer of skin

3. Some Australian frogs (Litoria and Cyclorana) secrete a proteinaceous skin layer and lipids during dry seasons on the savannah Litoria caerulea Hyperolius viridiflavus

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4. Some amphibians (mostly frogs and some Siren) can form a cocoon and estivate underground to avoid droughts and dry seasons

• Formed by repeated ecdysis where the skin doesn’t completely break away from the body but separates a bit as layers are added

• Opens at the nares so they can breathe

• One Australian hylid (Litoria alboguttata) can form a 24- layer cocoon in 21 days

– Many amphibians have water-conserving postures to reduce evaporation in dry conditions (most fold legs under the body)

• When they emerge, they will find damp spots and sprawl their legs so their ventral water-absorbing surface can collect water (seat patches in Bufo)

• Hormonal control regulates behavior similar to that which regulates drinking in other tetrapods

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– Freshwater crocodiles in Australia estivate for 3-4 months/year during droughts and go underground to reduce evaporation rates • Water is lost by evaporation, respiration, and excretion but evaporation is the route of greatest loss • Water storage by amphibians – Terrestrial frogs and salamanders hold between 20-50% of their body mass in their bladder – One Australian desert frog (Cyclorana platycephala, below) can hold 130% of its normal body weight in water in the bladder

Water-holding frog

• Water storage by reptiles

– Most use their bladder and those of desert tortoises may occupy more than half of their body cavity

– Some lizards use their stomach

– Lymph sacs in lateral abdominal folds of chuckwallas

– Baggy folds of skin around the legs of diamondback terrapins

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Nitrogen excretion – determined by habitat more than phylogeny

• Ammonia

– Aquatic animals – some frogs and all larvae – Must be diffused from gills and skin because kidneys don’t handle it well – Very toxic: Rana that excrete ammonia (most do not) die quickly when water is withheld – Xenopus (an aquatic frog) secretes ammonia most of its life but can switch to urea production while estivating during droughts

• Urea

– Water soluble and low toxicity – Produced by most amphibians • Some marine amphibians (none are truly marine but live in or near brackish water with) increase urea concentrations in their blood as salinity rises (61 frog and 13 salamander species) – Turtles and crocodilians

• Uric acid

– Not very soluble and requires little water to excrete – Most snakes and lizards – Some waterproofed frogs (waxy monkey tree frog) reabsorb 90% of water that is filtered by the kidney

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• Some reptiles exhibit anhomeostasis when solutes and waste in the body build up well above what is seen in most reptiles

– The desert tortoise (Gopherus agassizii) survives droughts by reabsorbing essentially all water during kidney filtration but still may lose 40% of their normal body mass while waiting for rain

• Urea concentrations in the blood and bladder can reach the highest levels known for vertebrates

• When it finally rains, they void the bladder of super concentrated urea, drink large amounts of water to replace it, and store it in their bladder until next rain

• On land, there is a big disadvantage from water loss

– Respiratory surfaces must be kept moist and water is lost to evaporation – Besides amphibians with cutaneous respiration, all terrestrial vertebrates have gas exchange surfaces in protected body cavities which greatly reduces evaporation

• Respiratory structures in amphibians include skin, lungs, gills, and buccopharyngeal cavity

• Most reptiles rely exclusively on lungs but there are exceptions

– Some turtles (soft-shelled turtles, Apalone) use cloaca and lungs – Cutaneous respiration is found in some other aquatic turtles

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• Gills

– Used only in water

– Tadpoles have them inside covered by operculum

– Larval salamanders have gills that vary in size and structure depending on environment

• Larger, more filamentous gills are found in those in stagnant water bodies and small gills are found in stream salamanders

• Buccal cavity and pharynx

– Reptiles and amphibians that remain submerged for long periods

– A small % of gas exchange in plethodontid salamanders

– Turtles (Apalone and Sternotherus) can collect enough oxygen to survive through skin and throat while staying submerged during hibernation

• Skin

– Many amphibians and a few reptiles

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– Ventilation (getting fresh supply of oxygenated water) of skin in water can be a problem and species can stay submerged longer in flowing water

– Plethodontid salamanders rely exclusively on skin and have no separation of venous and arterial blood

• This restricts them to cool environments and low activity

• Their oxygen intake is 1/3 that of frogs under similar conditions

• Tropical plethodontids are restricted to moving only on cool, rainy nights

• Lungs

– All reptiles and many terrestrial amphibians

– The left lung of most snakes is greatly reduced and only the posterior portion of it moves and respirates during feeding

– Turtles have a problem because they can’t move their shell- encased torso so they retract and protract their legs to assist air flow

– Some tadpoles have lungs but they never account for >30% of oxygen intake and they seem to function more as organs of buoyancy rather than respiration

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Physiology: Thermoregulation • Most amphibians and reptiles regulate body temperature by behavior and are able to keep it within a relatively narrow range

– Amphibians tend to have lower body temperatures because they lose moisture much more easily

• High temperatures and low humidity increase moisture loss • Many are nocturnal and/or limit activities to times when humidity is high

– Many reptiles bask to gain heat from sun and heated surfaces

– All metabolic processes are ultimately linked to temperature so body temperature regulation is complex for most species

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• All species have evolved an active temperature range where physiological function is maximized and chance of mortality is minimum

– A specific preferred temperature is most optimum

– Voluntary min and max – normal activity occurs and individuals maintain this range most of the time by normal behavior

– Critical thermal min and max – uses emergency measures and behavior to reach voluntary range and death results if not remedied soon

– The hypothalamus in the brain controls temperature regulation

• Heat is gained by radiation and conduction

– Terrestrial species can modify reflective properties or color of their skin to adjust body heat and this ability is under physiological involuntary control

– Smaller species have more limited physiological capabilities because of higher surface to volume ratios (outer surface area/inner volume) and water and heat are more easily lost

– Fossorial species gain heat by conduction from soil and undersurfaces of objects exposed to the sun (rocks)

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• Defense ability and fight-or-flight responses are determined by temperature in many species

– Green frogs (Rana clamitans) can leap 1 m within active temperature ranges but leaps are shortened below 10°C and above 25°C

– The Egyptian lizard Trapelus savignii will stand its ground and attack at low temperatures and is more likely to run from threats as temperatures increase

• Most salamanders have limited or no behavioral regulation of body temperature

– Moisture retention is imperative so basking isn’t an option for most

– Body temperatures are only a bit above ambient temperatures and physiological processes are adapted to lower temperatures

– Tropical plethodontids are limited to nocturnal activity and most species are restricted to temperate climates

• Most reptiles and frogs regulate temperature behaviorally to some degree

– Many frogs bask to gain heat and will move in and out of water to reduce heat

– Some frog species stay in contact with a moist substrate or standing water to constantly replace water lost at high temperatures (evaporative cooling)

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– Also, remember “waterproof” frog examples

• Physiological responses to reduce moisture loss function also to reduce body heat (Africa: Chiromantis) or enable them to endure greater body temperatures (S. America: Phyllomedusa)

• Some reptiles can regulate temperature by increasing heat production by muscular activity (this is how birds and mammals regulate)

– Pythons twitch their muscles while incubating egg clutches which raises their body temperature a few degrees above ambient so eggs develop and hatch quicker

• Leatherback sea turtles approach the endothermic conditions with:

1. An elevated metabolism 2. Large body size 3. Thick insulation 4. And, thermally efficient blood flow to skin and appendages (countercurrent heat exchange)

• They maintain body temperature from 25-26°C in water of 8°C

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Home Ranges • Area covered in everyday and seasonal activities

– Some areas may be heavily used (microhabitat where the individual has protection) while others may be rarely visited (breeding site visited once a year)

– Determines how individuals of a population are distributed throughout the landscape and many factors are involved:

1. Food, shelter, and escape routes 2. Mates and ovipostion (egg-laying) sites 3. Thermoregulation sites

– Although habitat use is highly variable among herpetofauna, there are some general patterns

• Simple, 2-dimensional home range

– We can calculate home ranges by area for terrestrial species that travel among points on a flat surface using the minimum polygon method

• Widely used for many groups of terrestrial animals so scientific literature is full of examples • Terrestrial plethodontid salamanders, 6-lined race runners, terrestrial turtles (box turtles) • Overlap in home ranges can be easily calculated

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– There may be differences by:

1. Gender 2. Age-class 3. Reproductive status 4. Season (dry vs. rainy or warm vs. cold season)

Individual home ranges of adult males (full lines) and adult females (dashed lines) of Liolaemus lutzae (an iguana) in two portions a study area in beach habitat in Rio de Janeiro

3-dimensional terrestrial

• Usually arboreal species

– They may use one or a few trees during a lifetime and home range may be small for tropical species that reproduce in trees – Hylid frogs, rough green snake, many tropical lizards and snakes

• With a bit more effort than the 2- dimensional approach, a home range measured in volume can be calculated

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• Semiaquatic species

– Have elongate home ranges along stream and lake shores

– Includes many frogs (Rana spp., Acris spp.), salamanders (Desmognathus spp.), turtles (Apalone spp.), and snakes (Nerodia spp., Regina spp.)

– Home ranges can change with fluctuations in water levels and erosion and movement of sand bars

• Aquatic species

– Usually large home ranges especially among marine species (sea snakes and turtles)

– Home ranges shift with fluctuating water levels and can have several over a life time if water bodies evaporate and individuals move permanently to other sites (painted turtles, red-eared sliders)

Movements of a green sea turtle

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• Some species have no defined home range – Shifts in areas of concentrated activity occur throughout life, usually following food sources

• Prairie rattlesnakes (Crotalus viridis) wander until an area of high prey density is found and move on when density drops below a point when captures are infrequent

• Water pythons (Liasis fuscus) of Australia follow dusky rat populations along rivers flood plains and levees as water levels fluctuate

• Bushmasters (Lachesis muta) move until they find a microhabitat that will attract prey (along fallen logs) and will stay there for days until a capture is made and several weeks after to digest

Paths travelled over a year for male timber rattlesnakes

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Prairie rattlesnake

Bushmaster

Water python

Territories • Portion of a home range actively defended against intruders

– Among herpetofauna, males usually have territories and females do not

– Males may defend areas of good forage and allow females to enter and mate with them

– Natural selection will favor individuals that can control important resources and they’ll more successfully contribute offspring to the next generation

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• Among amphibians, some frogs and salamanders are territorial but no caecilians

– Male frogs can define their territory by calls and may ward off intruders by displays or wrestling matches

– Occurs in frogs with extended breeding seasons (our ranids) or parental care (dendrobatids) but never in explosive breeders (spadefoot toads)

– Frogs are defending areas good for egg deposition where egg and larvae mortality will be least

– Most of what we know about salamander territoriality is from Plethodon spp.

• Males and females mark territories of good forage and shelter with pheromones

• Familiar individuals (those with neighboring territory) will be shown less aggression than new individuals as long as they keep a distance

• Attacks can occur and are directed at the tail (important source of energy storage) and nasolabial grooves (transmit chemical signals)

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• Among reptiles, territoriality is seen often in lizards and crocodilians

– Sceloporus spp. will defend a foraging area and territory size will depend on food density, the more dense the food the smaller the territory

– Lizards of suborder Iguania and family Gekkonidae will mark territory in a variety of displays including push-ups, head bobbing, dewlap expansion

• Intruders may be defended against by combat (biting, wrestling), displays (above), or avoidance (chemical signal)

• Teiidae (racerunner, whiptails), Lacertidae (large family of Old World lizards), Anguidae (glass and alligator lizards), and Varanidae (monitor lizards) show no territoriality because they are active, wide-ranging foragers

– Many crocodilians will defend nest areas

• Aggregations of individuals (breakdown of territoriality)

– Centered around scarce resources during brief periods of time – In amphibians:

• Adults in water bodies during breeding events (spadefoot toads and ambystomatid salamanders)

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• Tadpoles of several species may school to avoid predation

• Terrestrial salamanders may cluster in moist areas during extreme droughts

– In reptiles:

• Many snakes (garter snakes, rattlesnakes) cluster for overwintering and mating (garter snakes)

• Some fence lizards cluster in rock crevices to overwinter

• In rocky terrain, lizards and snakes may cluster and lay eggs in talus mounds

Garter snakes emerging from hibernacula Marbled salamanders captured in in the spring pitfall trap on the way to breeding pond

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Movements, Homing, and Migration • Most herptofauna need to move over relatively long distances (compared to home range movements) during some time of life for reproduction, overwintering, water, food, or new territory

• Mass movements are seen in many species

– Ambystomatid salamanders and many frogs move to and from ponds to breed on nights with favorable weather and metamorphs will leave ponds en masse

– Sea turtles and some freshwater turtles arrive at beaches by the thousands over a few nights to synchronize hatching and overwhelm predators of eggs and hatchlings

• Dispersal – undirected movement to unknown locations, usually by juveniles

– Reasons to disperse include:

• Juveniles finding a home • Habitat instability • Intraspecific competition • Inbreeding depression

– Costs:

• Increased predation risk in unknown area • Difficulty finding resources • Potential aggression from unfamiliar conspecifics

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– Benefits:

• May discover better resources • Increased likelihood of outbreeding • Possible reduction in competion

– Juveniles are more likely to disperse in dense populations and often times settle in marginal habitat

– Amphibian metamorphs and sea turtle hatchlings disperse from natal sites with seemingly no direction but return to the same sites later to breed

• Homing – ability of displaced individuals to return to their original location

– For this to occur, animals must be able to sense direction by visual, olfactory, auditory, or magnetic cues

– Landmarks (visual)

• Repeated use of the same perches, forage areas, and retreats within home ranges allow most small, relatively sedentary herpetofauna to know their surroundings

• Some lizards (Anolis spp.) can observe an area from an elevated perch and select the appropriate microhabitat to orient to

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– x-y orientation (sun and linear landmarks)

• Many semi-aquatic and aquatic species use the shoreline as an x-axis and set a y-axis at a 90° angle using the sun to orient themselves in the water

• Experiments have shown that adults and larvae can orient themselves perpendicular to the shore as long as they can see the horizon

• Important for:

– Guiding them to breeding sites – Escaping predators by jumping directly out from the bank and the ability to return – Directing metamorphs at time of emergence

– Chemical cues (olfactory)

• Some toads (Bufo spp.) and salamanders (Plethodon spp., Taricha spp., Ambystoma maculatum) home in on natal ponds by smell after being displaced up to 200 m

• Experiments involved blinding some individuals and severing olfactory nerves of others

– Magnetic orientation

• Eastern red-spotted newts seem to posses a homing system based on variations in the magnetic field and sunlight (one of the best salamanders at homing in on natal ponds)

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• Sea turtles navigate the open ocean using an internal compass

– As hatchlings, they orient to the water as the moon and stars reflect off the ocean then orient themselves perpendicular to incoming waves

– To return to nesting beaches, a combination of cues seem to aid them, including Earth’s magnetic field and information from trade winds blowing off islands

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Communication • All herptofauna must interact with other organisms in the environment, especially their conspecifics, with various types of cues:

– Visual – Chemical (nasal and vomeronasal) – Acoustic – Tactile

• Signal production and signal receptor are tightly linked evolutionarily for precise intraspecific communication

• In many species, senses are heightened and closely tuned to detect a conspecfic signal during the reproductive season

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• There are obvious benefits to communicating (mate attraction, predator warning, etc.) but there are also some costs: – Could lower survival – if a conspecific can locate you, there is probably a predator that can also

– Energetic cost – some communication (frog vocalizations) requires significant energy • A brief overview of communication among taxa by type: 1. Visual

– Found among most groups but more rudimentary in amphibians

– Can be movements (head bobs, open mouth) or color (many reptiles are sexually dimorphic and can see color)

2. Acoustic

– Most developed in anurans

– Also, crocodylians (slapping tail against a surface, mother- offspring communication), some lizards (geckos grunt), and snakes (rubbing scales together)

3. Chemical

– Volatile (nasal) or surface adherent (vomeronasal) odors from glandular secretions

– Most developed in salamanders and skinks

– Also, some snakes, iguanids, and caecilians

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4. Tactile

– Rub, press, or hit body parts

– Common in snakes and turtles

– Some lizards and salamanders

• Caecilians

– Most social communication is chemical

– They have a chemosensory organ (a tentacle) just anterior to the eye that has internal connections to their Jacobson’s organ

Male plethodontids rub their mental gland (MG) on females and other surfaces to smear pheromone; premaxillary teeth abrade skin and introduce the chemical to the female’s system

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– While burrowing, they close nostrils and detect with the tentacle

– Mate location probably depends on pheromones (chemicals secreted to elicit a specific response in another individual)

• Salamanders

– Rely heavily on chemical cues for courtship and to distinguish among species

– Odors identify: sex, reproductive status, and stimulate females

– Pheromones are produced in glands found only in males and they usually atrophy during the non-breeding season

• Courtship glands are very common in Salamandridae and Plethodontidae – Males of Notophthalmus (newts) have a genial gland on either side of their head and wafts the smell with tail undulations toward a receptive female • If she is receptive, he will deposit a spermatophore and she will accept it • If the female isn’t receptive, he’ll grasp her neck with his hindlimbs for about 3 hours and rub genial glands against her snout and she will eventually absorb the pheromone and accept the spermatophore

Red spotted newt courtship

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– Plethodontid salamanders have mental glands (diagram) and caudal glands on the dorsal base of their tail

• Courtship displays are elaborate and vary by species

• Tactile signals (nudge, but, slap, rub, bite) are an integral part along with pheromone release

• Frogs

– Most communication is acoustic signals in 4 categories:

1. Advertisement – courtship, territorial (defense), and encounter (recognition); all male

2. Reciprocation – female in response to male courtship call (rare)

3. Release – male to male indicating a mistake has been made in amplexus; common among explosive breeders

4. Distress – loud screams from females during a predatory attack

– Vocal sac structure varies among species

– Generally, females ignore heterospecific calls

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– Some species use visual signals to signal courtship or territory

• Hand waving, foot flagging, leg stretching, toe undulations, body raising and inflating, color changes

• In one leptodactylid, Hylodes asper, the male vocalizes then raises his light colored foot in a flagging motion so it stands out against the dark background of the stream and rocks behind (combination attracts the female)

• In some species (brightly colored dendrobatids) females may use colorful body parts to signal territory

Hylodes asper

• Turtles

– Usually a combination of visual and chemical signals

– Male tortoises use head bobs and swaying to identify one another

– This may escalate into butting or biting if territory is in dispute

– Desert tortoise males may start a confrontation, stay in the same burrow overnight, and emerge the next day and continue the dispute

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– When a female is encountered, the male will bob and sway and the female will retreat

• The male will follow and attempt to mount her after biting and ramming stimulates her

– Emydid turtles (pond turtles) display patterns and colors on forelimbs, neck, and head to signal one another

• Patterns are species specific and females recognize males when they display in front of them

• While face-to-face, the male will bump heads with the female and attempt to position himself on top

• Next, the male will rapidly vibrate his elongated claws under the female’s chin and rapidly move his jaw in a chewing motion

– Many turtles (musk turtles) have Rathke’s gland on the bridge of the shell that produce aromatic chemicals and they are able to find and follow one another in water this way

– Some have mental glands that are active during the breeding season

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• Crocodylians

– Mostly visual signals (close range) and some auditory (long range)

– A male will defend his territory with a series of visual signals

• First, a resident will raise his head and arch his tail partially out of the water and approach the intruder

• Chases, lunges, and real or mock fights may ensue

• After the chase, the resident will inflate his body

• Alligators will slap the water with their head to create a splash

– Auditory signals include bellowing, juvenile grunts, and slapping sounds

• Male and female alligators bellow with loud, low-frequency bellows during the breeding season and after egg deposition

• Male and females use cough-like calls for close range communication during courtship

• Juveniles grunt when distressed and most adults will move toward the sound

• Adults can also produce similar grunts that cause juveniles to move toward them

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• Tuataras

– All visual and tactile signals

– Males defend territory (a burrow) by inflating his body, elevating the dorsal crest, and darkening the skin

• Next, the resident will shake his head laterally; if this doesn’t ward off the intruder they will face each other but look in opposite directions • They will rapidly open and close their mouths then begin chases and tail-whipping

– Females will respond to males with a head nod and he will begin an extremely slow, stiff-legged walk toward her

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• Lizards

– Iguania (anoles, chameleons, iguanas, and relatives) use more visual cues and rely little on chemical and tactile signals

– Most are territorial and sit-and-wait foragers and rely more on vision

– Color of dewlaps, heads, and patches on lateral and ventral surfaces of the body are often used

– Anolis uses head bobs and dewlap displays in territorial and courtship displays and females select more brightly colored males

– Males of some species will attack the female of the same species if they are painted with the same ventral colors as males (Sceloporus undulatus, Eumeces laticeps)

– In some highly territorial species, females will undergo rapid color change as she becomes sexually receptive

• Nearby males notice the change and approach her • After mating she retains her color and rejects other males

Sceloporus sp.

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– Scleroglossa (geckos, skinks, snakes, and relatives) use chemical cues more than Iguania

• Most are roving foragers and not likely to have territories • Our Eumeces (skinks) complex use chemical signals to a great extent

– Males can distinguish among the various species, by sex, and if a female is in breeding condition

– Males follow trails of females during breeding season

– When the males approaches a female, he will start tongue-flicking her body until he reaches the cloaca

– The female will secret a cloacal pheromone to signal the male and copulation begins

• Auditory signals are very limited among all lizards; geckos use them to signal nightly feeding territories

• Snakes

– Chemical cues for long-range and tactile for close-range

– They have a number of glands but the most used are paired cloacal glands for trailing and defense (horrible smelling to most predators, including humans)

• Females have glands on their dorsal surface that produce pheromones during the breeding season and cause the male to begin courtship activities

• Pheromones are species and gender specific

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– Once a male recognizes a female, tactile cues begin and occur in 3 phases: chase, alignment, and intromission-coitus

• Males may rub their chin on and bite the female

• Snakes with vestigial limbs (Boidae) will use the pelvic spurs to stimulate females near the cloaca

– Male combat occurs in viperids, colubrids, boids, and elapids and involves chemical and tactile cues

• Males will determine if the other conspecific is male by chemicals • If neither retreat, they will glide past one another with heads raised and eventually start “wrestling” in an attempt to pin the others head until dominance is established

Male-male combat in brown snakes of Australia

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Foraging

• Herpetofauna are broadly categorized as sit-and-wait or active foragers

– The ancestral condition appears to be sit-and-wait foraging with active foraging evolving later in one or a few evolutionary events

• The importance is that herpetofauna may be constrained by evolutionary traits when it comes to adapting to food sources (i.e., an active forager will always be an active forager)

• Many morphological, behavioral, and physiological traits evolved together to support a foraging strategy (metabolic rate, defense mechanism, reproductive habits, etc.)

– Sit-and-wait: sedentary, visually oriented, cryptic morphology

– Active: in relatively constant motion, visually and chemically oriented, swift reaction to predators (rapid flight defense)

• Prey detection can be:

– Visual – Chemosensory (olfaction, vomerolfaction, and gustatory) – Auditory – Thermal – Tactile

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• Visual

– Most utilized by sit-and-wait predators

– Usually requires binocular location of prey

• Chameleons are an exception with independently moving eyes

– Many diurnal and nocturnal species (horizontal or vertical elliptical pupils usually signifies more nocturnal activity) – Most species have specific prey sizes and shapes as cues and will not feed on just any small, moving object, though there is a range of selectivity

• Marine toads (Bufo marinus) will ingest about any small object moving within its range of vision (living or not) • Salamandra salamandra from Europe requires very specific cues to elicit an attack

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• Chemosensory

– Olfaction relays long-range information (presence and general location)

– Vomerolfaction (Jacobson’s organ) relays short-range information and is most important

– Gustation acts as a last discriminatory sense

– Many salamanders, lizards, and snakes that actively forage switch between visual and chemical prey detection

• Skinks use vision in open habitat and switch to chemosensory detection in leaf litter and dark crevices

• The Italian cave salamander (Hydromantes italicus) uses solely chemical cues to detect prey in complete darkness

– Snakes rely heavily on chemoreception to detect prey and some species (garter snakes) will not forage if the sense is disabled even if they clearly see the prey item

– Taste is not used to locate prey but an item may be rejected once in the mouth because of it

• Also, tactile cues (spines or irritating hairs) may cause prey release

Italian cave salamander

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– Once the clade Scleroglossa (geckos, skinks, snakes, and relatives) broke from the ancestral Iguania (anoles, chameleons, iguanas, and relatives), chemosensory detection of prey evolved

• This made a large set of prey available (nonmoving and hidden prey such as insect larvae)

• All chemosensory structures were and are present in the Iguania, but they’re used almost exclusively for social communication

• One exception is herbivorous iguanas that use taste to discriminate among food types

• Auditory

– Likely used in a wide range of herpetofauna but not well- documented

– Some anecdotal observations include marine toads moving toward a smaller, calling Central American frog (túngara frog) and the Mediterranean gecko that will locate calling male crickets and eat female crickets as they approach

– Snakes, salamanders, and caecilians have no external ears so they rely heavily on seismic vibrations for predator and prey detection

– Frogs and salamanders possess a special pathway to detect seismic vibrations called the opercularis system

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• Forelimbs are linked to the inner ear by the opercularis muscle that extends from the scapula to the opercular bone of the otic capsule

• Salamanders are twice as sensitive as frogs to low frequency ground-transmitted vibrations

– Snakes detect seismic vibrations via the lower jaw (the quadrate-columella bone connects to the inner ear)

• Thermal

– Some snake groups including most boas and pythons and all vipers in the sub-family Crotalinae (Crotalus, Agkistrodon, Lachesis, Bothrops, etc.)

– Pits sensitive to long wavelength infrared light (radiant heat) face forward on the face either along the jawline in labial scales (boids) or in loreal scales (vipers)

– Specialized for nocturnal foraging on mammals and birds

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• Tactile

– Mechanoreceptors of various types in the skin relay info about surrounding possible prey – Lateral line systems in aquatic salamanders; some species uses it exclusively to locate and identify prey – Some turtles (alligator snapping turtle) use tactile cues detected in and around the mouth to trigger feeding

Prey Capture and Ingestion • With few exceptions, herpetofauna swallow prey whole and display a wide array of methods to subdue them

• Biting and grasping

– Most common method

– Some strike from ambush and others actively stalk prey

– Some use lures: juvenile viper’s tail, horned frog’s foot, alligator snapper’s tongue

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– Most swallow whole without processing (chewing) but exceptions include some lizards (broad-headed skinks) that crush exoskeletons of invertebrates and snakes that puncture toads to deflate them

• Constriction

– A specialized bite-and-grasp method used by many snakes and some aquatic salamanders (amphiumas)

– Prey is bitten and held while a loop of the body is slung around it

• After several more loops are around the prey, the snake continually applies pressure until the prey suffocates or blood circulation is restricted from vital areas

– One of the most specialized constrictors are the filesnakes (Acrochordus sp.)

• They attach their tail to an underwater anchor (roots) and strikes then constricts fish that come by

• Its scales are especially rough to hold slippery fish

Filesnakes

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• Injected venom

– All Elapidae, Viperidae, Helodermatidae (gila monster), and some Colubridae

– Beneficial because:

1. Lessens chance of injury to the predator 2. Larger prey items can be subdued 3. Digestive enzymes also are injected that begin tissue breakdown

– All venom delivery systems must have 4 things: venom glands, muscles to force venom from the glands, ducts to transport it to teeth, and fangs

– Fangs of colubrids and helodermatids have simple grooves on one side of the tooth

– Vipers and elapids have closed canals

Boomslang - Colubridae

Gaboon viper - Viperidae

Mamba - Elapidae

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– Viperids and some elapids strike and release prey while most elapids, colubrids, and helodermatids bite and chew to ensure envenomation

– Depending on species, venom causes massive tissue damage (prey goes into shock) or neurological collapse (never impulse transmission is blocked and muscles stop)

• Projectile Tongues

– Most frogs capture prey with their tongue

• It’s attached at the front of the mouth and is slung outward like a catapult

• The free end is heavy and stretches the tongue twice its length and prey items stick to the end

– Many lungless salamanders use their tongue to various degrees depending on species

• Projectile tongues evolved several times among salamander groups

• As in frogs, the projectile force stretches the tongue, 40-80% of body length

– Chameleons have the most specialized tongue projection system; some can stretch their tongue twice their snout-vent length

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• Filter feeding

– Most tadpoles eat algae and protists strained from water

– A large buccopharyngeal cavity and a complex system of papillae filter small items and direct them to the esophagus

• Suction feeding

– Aquatic salamanders, pipid frogs, and some turtles

– Most have large buccal cavities that are rapidly expanded as the mouth opens (vavular nostrils are closed to seal the cavity)

– Nearby prey are sucked into the mouth

The matamata turtle in South America has the most advanced suction feeding system among herpetofauna

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Defense

• Herpetofauna must risk predation to gather food and engage in social interactions

– In all these activities, species must balance the tradeoff between risk of exposure and need to secure resources

– Generally, smaller species will retreat to refuges in various ways depending on the perceived degree of threat

• In Anolis lizards, individuals of arboreal species that use lower perches will retreat when a predator is at a greater distance compared to those that use higher perches

• Cryptic species will allow predators to approach more closely than those that are not cryptic

• Male broad-headed skinks will allow predators to get closer if he is with a female and lets the female escape first to the refuge (the cost of losing a mate is high)

• Escaping detection

– Prey have 2 options to avoid detection by predators:

1. Interfere with predator’s ability to use cues (visual, olfactory, etc.) 2. Be inactive when predators are searching for food

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– Many herps are nocturnal and avoid diurnal bird species, a primary group of predators

• The tradeoff is giving up food sources (diurnal insects) and lower temperatures which will slow performance

• There will still be some nocturnal snakes and bats that may prey on some prey species

– Many prey species are cryptic in coloration and/or morphology to avoid visually oriented predators (birds, other herps, some mammals)

• One tradeoff is they often must be completely immobile and allow predators to approach closely to avoid detection

– Color and pattern usually varies geographically within species to match local environments

Geographic variation in rock rattlesnakes

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• In some species, there is great color and pattern variation within a population so predators cannot form a reliable search image

• Aposematic coloration

– Many amphibians are noxious or lethal and have bright coloration to warn predators that serious injury may result if they attempt to eat them

– Some species have a particular posture, or unken reflex, that they use with bright colors to further warn predators

Mexican burrowing toad Budgett’s frog

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• Mimicry

– When one species (non-toxic/venomous mimic) resembles another species with aposematic characteristics (toxic or venomous model) and deceives predators into not attacking

• This is Batesian mimicry where one species receives protection but isn’t really harmful

• There is also Mullerian mimicry where 2 or more species are truly dangerous and are marked similarly so they reinforce the danger to predators

Noxious red-cheeked salamander (Plethodon jordani, large one) with harmless imitator from a different genus (Desmognathus imitator)

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– Some reptiles mimic toxic invertebrates and predators avoid them although they’re non-toxic

• Escaping predator approach

– Many species must move while foraging and expose themselves to predator detection

Juvenile Kalahari lizard acts and resembles a toxic carabid beetle

– Some escape to burrows and inflate themselves inside so they are very hard to extract (chuckwalla in the Southwest)

– Most frogs jump to avoid predators and aquatic species jump into water or bury themselves in mud

– Some arboreal lizards and frogs will parachute to safety

Flying lizard, Draco sp. Fringe‐limbed treefrog

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• Threat displays

– Some displays may cause predators to give up the attack approach

– The rattling and hissing of snakes and some lizards deter predators, especially if coupled with expanded body parts

• Hood of a cobra • Cottonmouth with open, white mouth • Rattlesnake rattle

– Some frogs open their mouths, and one, the horned frog, will strike a predator and hold on with massive jaws

• Skin, armor, and spines

– Turtle shells with bony dermal plates provide great resistance to predators

– Crocodylians and some lizards have scales with bony osteoderms beneath as heavy armor

– The spines of horned lizards have been known to puncture and kill predatory snakes (coachwhips) after ingestion

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– The jaws and claws of large-bodied turtles and lizards inflict painful wounds and cause predators to release

– The newt Echinotriton andersoni will display and show its brightly colored tail to warn predators and if they attack, the spines along the flanks (projections from the ribs) can puncture and deliver poison

• Chemical defense

– Granular and parotoid glands of amphibians produce mildly noxious to lethal poisons

• The glands can be concentrated in one area and the animal will present this to the predator so it must take that part into its mouth first

• Some salamanders (2 and 3-lined salamanders) will lash their tails at predators where the poison is concentrated

Colombian 4-eyed frogs presents their poisonous rear to predators

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– Some salamanders (below) can spray poisons up to 200 cm from pressurized glands

– Some produce glue-like chemicals that is very irritating to predators (our slimy salamanders)

– These various types of chemicals can be put into 4 categories:

1. Biogenic amines – affects function of the vascular and nervous systems (serotonin, epinephrine, dopamine)

2. Peptides – modify cardiac function (heart races, possibly stops)

3. Bufodienolides – disrupts normal cellular transport and metabolism (many harmful effects)

4. Alkaloids – similar to bufotoxins

– Many of these compounds come from arthropods (especially ants) that amphibians eat

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• Feigning death

– Occurs in some frogs, salamanders, lizards, and snakes

– Many are arboreal species that escape by falling from trees and are completely still once they heat forest floor

• We assume this is so they are cryptic and get lost in the leaf liter below

– Our hognose snake does the most elaborate display

• Many times it defecates on itself during the display and the feces probably contain toxins from toads that it eats

• Tail displays and autotomy

– Salamanders may display their tail to show predators that they are toxic

– Some snakes and lizards will display their tail to distract the predator from vulnerable parts of the body and possibly escape after the initial attack

– Many salamanders, most lizards, and a few snakes lose their tails during attack and the predator is distracted most of the time

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Herpetofauna and Humans

• Herpetofauna, like other animal groups, have suffered species extinctions and population reductions from human activities, especially over the past century

• Habitat loss and modification by humans is the most visible and probably greatest problem for herp species

– Natural ecosystems converted to farm land – Habitat lost to housing, commercial, and infrastructure (roads, etc.) development – Deforestation from the taiga to the tropics – Drainage of wetlands for irrigation and development

• Pollution can be a cause of species decline in some areas

– Pesticides and herbicides that wash from agricultural fields can kill up to 99% of frog tadpoles

– Acidification of habitats from burning coal has occurred in many heavily industrialized areas of the world

• Sulfur and nitrogen compounds become airborne and mix with precipitation; this forms sulfuric and nitric acid

• In most developed countries, regulations have alleviated the problem but still a big problem in countries like China and India

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• Normal rain has some carbonic acid and a pH of about 5.6- 5.8; acid rain may have a pH from 3.0-4.0

• Most amphibian species suffer >50% loss of eggs or aquatic larvae at a pH of 4.5

• Diseases have affected some groups and human activities are related to high incidence of infection

– Many sea turtles, especially green sea turtles, are infected with fibropapillomatosis (GTFP)

• Large non-cancerous tumors grow on young turtles and eventually hinder swimming, feeding, and internal organ function

• Infection rates vary by body of water but are as high as 92% (Kaneohe Bay, Hawaii) at highly disturbed sites

• We’re not sure exactly what causes it but possibly a virus associated with pollution from sewage in bays with little water circulation

• Juvenile turtles are infected when they return to near-shore areas to breed and feed

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– The chytrid fungus causes chytridiomycosis in many frog species and it is quickly spreading

• It affects keratin in frog skin and produces a toxin that kills about 80% of those infected

• In Australia, it was unknown in the wild before 1978 but now infects most frog species in moist, temperate habitats in the east (6-8 species have gone extinct)

• The pet trade along with various environmental stresses have caused the disease to spread rapidly around the globe and become very lethal

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• About 1/3 of the world’s 6,060 amphibian species are threatened with extinction

• Harvesting for food or the pet trade has been a major contributor to herp species declines

– The European pet trade overharvested its native tortoises and those in adjacent Asia and Africa (Testudo spp.)

• Next, they began importing box turtles (Terrapene spp.) from the U.S. causing local population declines until regulations were enacted to greatly limit harvest

– The Chinese highly prize turtle meat and pay up to $1,000/kg for wild-caught individuals of some species

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• Many of their 90 species of turtles are endangered because of overharvest

• They have >1,000 large turtle farms (worth $1 billion) but even this can’t meet the demand

– Large lizards (Varanids (monitors) and iguanas) and crocodilians are overharvested in developing countries

• By 1967, the American alligator was on the brink of extinction and was placed on the Endangered Species List

• The population has recovered and now there are >1 million

Chinese turtle market

Attempt to smuggle turtles in China

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• Sea turtles

– All 7 species of sea turtles are endangered

– They are still taken for meat in Latin America, southeast Asia, and India

– Eggs are eaten, babies are stuffed as souvenirs, and hawksbill shell is made into jewelry and other products

– Many die in fishing nets and choke after swallowing plastic bags they mistake for jellyfish

– In places where they aren’t harvested much of their nesting grounds have been covered by human development

Hawksbill shell and products

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Exotic Species

• Exotic species are those that are taken from one zoogeographic region and placed in another

– In most cases, the new species does not survive well in a new area but when they are successful, ecological imbalances occur

– Sometimes, herp species are affected and decline, in other cases they cause the decline of other species

– On many islands, introduction of rats, mice, cats, pigs, goats and mongoose have led to the extinction or decline of many herp species (the tuatara in New Zealand is about gone)

• Cane toad (Bufo marinus)

– Native to much of South America and Mexico

– Was introduced in early 1800’s to many areas that grew sugar cane to control the cane beetle

– Now, it is found in about all areas of the tropics and semi-tropics (Florida)

– A huge problem in Australia where it eats and outcompetes native frog species

– The tadpoles are toxic and adults have poison glands behind their head that ooze a toxin that can kill predators (of course, the chytrid fungus does not affect it a bit)

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The voracious marine toad

I found these near some of the highest elevations in Puerto Rico. They don’t breed away from the coast (I never heard one calling male), so they could only have been there to forage. It’s a very good thing all other frog species in the mountains are tree frogs which live and breed in elevated locations.

Introduced to Guam in 1950’s and had spread over island by 1970 Brown Tree Snake (Boiga irregularis) Caused extinction in 12 native species of birds and several others are barely hanging on

Over 1,200 power outages due to the snake since 1978

Introduced or seen on 9 other Islands including Hawaii; also Texas

We now use trained dogs to sniff them out on incoming airplanes at airports.

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• The common coqui frog, Eleutherodactylus coqui, from Puerto Rico

– First recorded on Hawaii (that previously had no frogs) in 1988 after being transported there in ornamental plants

– By 1998, it was found at 8 sites on Hawaii and 12 on Maui

– By 2001, 124 sites on Hawaii and 36 on Maui

– They can occur at densities of 20,000/hectare and the mating call of a large chorus is about deafening

– Also, they eat massive quantities of invertebrates which causes declines in populations of native birds

• In Mississippi, many herp species have declined because of habitat loss

– Many of the declines are because of the near loss of the longleaf pine ecosystem that dominated the lower half of the state

– Most of the longleaf area was cleared in the boom years of southern lumbering from 1880 to 1920

• Foresters thought the timber would naturally replace itself like many other tree species that dominated other forested regions in the Southeast

• They quickly saw this did not happen as smaller trees with lesser quality wood soon dominated

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Endangered and threatened species of Mississippi

AMPHIBIA Endangered AMPHIUMA PHOLETER ONE‐TOED AMPHIUMA ANEIDES AENEUS GREEN SALAMANDER EURYCEA LUCIFUGA CAVE SALAMANDER GYRINOPHILUS PORPHYRITICUS SPRING SALAMANDER RANA SEVOSA DARK GOPHER FROG

Threatened AMBYSTOMA TIGRINUM TIGER SALAMANDER CRYPTOBRANCHUS ALLEGANIENSIS HELLBENDER HEMIDACTYLIUM SCUTATUM FOUR‐TOED SALAMANDER PLETHODON AINSWORTHI BAYSPRINGS SALAMANDER PLETHODON VENTRALIS SOUTHERN ZIGZAG SALAMANDER PLETHODON WEBSTERI WEBSTER'S SALAMANDER PSEUDOTRITON MONTANUS MUD SALAMANDER PSEUDOTRITON RUBER RED SALAMANDER

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REPTILIA Endangered CARETTA CARETTA LOGGERHEAD CHELONIA MYDAS GREEN TURTLE DERMOCHELYS CORIACEA LEATHERBACK DRYMARCHON CORAIS COUERI EASTERN INDIGO SNAKE ERETMOCHELYS IMBRICATA HAWKSBILL FARANCIA ERYTROGRAMMA RAINBOW SNAKE GOPHERUS POLYPHEMUS GOPHER TORTOISE GRAPTEMYS FLAVIMACUATA YELLOW‐BLOTCHED MAP TURTLE GRAPTEMYS NIGRINODA BLACK‐KNOBBED MAP TURTLE GRAPTEMYS OCULIFERA RINGED MAP TURTLE HETERODON SIMUS SOUTHERN HOGNOSE SNAKE LEPIDOCHELYS KEMPII KEMP'S OR ATLANTIC RIDLEY PITUOPHIS MELANOLEUCUS LODINGI BLACK PINE SNAKE PSEUDEMYS POP 1 MISSISSIPPI REDBELLY TURTLE

With 27 listed as threatened

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