Reproduction in Amphibians

Reproduction in Amphibians

Amphibian Eggs

• Amphibian eggs are non-cleidoic, meaning they lack a shell.
• They must be laid in a moist environment to prevent desiccation.
• Features of amphibian eggs:
  • Embryo
  • Yolk plug
  • Perivitelline fluid
  • Vitelline membrane: surrounds the embryo and yolk sac before fertilization.
  • Jelly capsule: provides mechanical protection and prevents desiccation.

Primitive Mode of Reproduction

• The primitive reproductive mode involves a return to water for reproduction.
• Example: Common frog (Rana temporaria)

Modifications of Reproduction

• Amphibians exhibit various modifications to their reproductive strategies.

1. Loss of Larval Stage

• Some species have lost the larval stage.
• Example: Whistling frog (Eleutherodactylus martinicensis)

2. Loss of Adult Stage (Neoteny or Paedomorphosis)

• Some species exhibit neoteny or paedomorphosis, where they retain larval characteristics into adulthood.
• Almost exclusively seen in salamanders.
• Example: Axolotl (Ambystoma mexicanum)

3. Addition of a Non-Reproductive Terrestrial Stage

• Some species, like the North American Notophthalmus, have a non-reproductive terrestrial stage called an eft.
• Adult (aquatic) → Eft (terrestrial): The eft stage can persist for up to 7 years or may not occur at all.
• Example: Red-spotted newt (Notophthalmus viridescens)

Mode of Reproduction: Aquatic Eggs

• Eggs are laid in various aquatic environments:
  • Freshwater (ponds/lakes): e.g., leopard frog (Rana sphenocephala)
  • Brackish water (estuaries, beaches): e.g., green toad (Bufo viridis)
  • Flowing water (streams/rivers): e.g., tailed frog (Ascaphus)
  • Small collections of water (e.g., bromeliad tanks): e.g., Trinidad golden tree frog

Mode of Reproduction: Eggs on Land

• Eggs are laid in terrestrial environments:
  • Under stones or other cover: tadpole nutrition provided by yolk (e.g., Caribbean whistling frogs Eleutherodactylus spp.)
  • Under stones or other cover: tadpoles make their own way to water (e.g., Salamander Desmognathus spp.) or develop on land (feeding on yolk) via direct development.

Foam Nests

• Foam nests are used for egg deposition:
  • Foam nests over water: e.g., Asian brown tree frog (Polypedates leucomystax)
  • Foam nests in burrows, with non-feeding or provisioned tadpoles: e.g., Leptodactylus.

Variable Modes of Reproduction

• Some frogs can lay eggs both on land and in water.
• Example: Hourglass treefrog (Dendropsophus ebraccatus)
• This plasticity could help researchers understand how terrestrial reproduction evolved in vertebrates.
• Reference: Touchon JC, Warkentin KM. 2008. Reproductive mode plasticity: Aquatic and terrestrial oviposition in a treefrog. PNAS 2008 105: 7495-7499.

Variable Hatch Times

• Red-eyed tree frog (Agalychnis callidryas) larvae sense vibrations from egg predators and hatch prematurely.
• Trade-off between aquatic/arboreal predation risk.
• Reference: Cohen, K. L. M. A. Seid, K. M. Warkentin. 2016. How embryos escape from danger: the mechanism of rapid, plastic hatching in red-eyed treefrogs. J. Exp. Biol. 219: 1875-1883; doi: 10.1242/jeb.139519.

Mode of Reproduction: Eggs in Oviducts

• A. Ovoviviparous:
  • Nutrition provided by yolk.
  • Examples: some salamanders, a few anurans
• B. Viviparous:
  • Nutrition provided by oviducal secretions.
  • Examples: African toad Nectophrynoides spp.
  • Specialized lining of oviduct (matrotrophy) in some caecilians with special teeth that are shed after birth.

Viviparity in Amphibians

• Viviparity has evolved at least 4 times in caecilians.
• Rare in anurans.
• Rare in salamanders (Salamandridae only).
• Intrauterine cannibalism occurs in some species.
• doi:10.1371/journal.pone.0115884

Breeding Cycles: Stimulus

• Temperate regions:
  • Seasonal hypertrophy of gonads.
  • Rise in temperature in spring stimulates the anterior pituitary gland to release hormones that stimulate gonads.
• Tropical seasonal/dry:
  • Occurrence of rain (annually or erratically).
• Tropical moist:
  • Breeding may be continuous, with a peak at the wettest time of year.
• Physiological and activity cycles may not be the same, especially in the tropics.

Location of Mates

• Caecilians:
  • Chemical cues (solitary, fossorial, blind and deaf but with good sense of smell).
• Newts:
  • No external ears, olfactory cues are important (e.g., smell of decomposing pond vegetation).
  • Reference: Joly P, Miaud C. 1993. How does a newt find its pond’–the role of chemical cues in migrating newts (Triturus alpestris) Ethology Ecology and Evolution 5:447–455.
• Smooth newts (Lissotriton vulgaris) preferentially orient toward calls of toads favoring similar breeding ponds.
  • Reference: Pupin, F., et al. (2007) Discrimination of toad calls by smooth newts: support for the heterospecific attraction hypothesis. Animal Behaviour, 74, 1683-1690. doi:10.1016/j.anbehav.2007.03.020
• Eastern red-spotted salamander (Notophthalmus viridescens) uses true navigation.
  • Reference: Deutschlander, M. E., S. C. Borland & J. B. Phillips. 1999. Extraocular magnetic compass in newts Nature 400, 324–325. https://doi.org/10.1038/22450

Location of Mates in Anurans

• Anurans:
  • Olfactory, auditory (calling).
  • Sometimes visual (e.g., foot-flagging).
  • Examples: Staurois (Borneo), Micrixalus (India), some Neotropical species.
  • Mostly in noisy environments.

Courtship

• Caecilians:
  • Unknown.
• Newts:
  • Visual, tactile, and chemical cues.
  • Amplexus in a few only.
• Frogs:
  • Auditory (exclusive to anurans).
  • Amplexus important, during which tactile, olfactory, and auditory cues operate.
  • Examples: Polypedates leucomystax, Triturus cristatus, Calotriton arnoldi, Notophthalmus viridescens

Types of Amplexus in Anurans

• Inguinal
• Cephalic
• Axillary
• Head straddle
• Glued
• Dorsal straddle
• Independent

Nuptial Excrescences in Males

• Some male amphibians develop nuptial excrescences

Fertilization and Development

• Caecilians:
  • Internal fertilization with the aid of a phallodeum.
  • Few yolky eggs.
  • Aquatic eggs and larvae, terrestrial eggs and direct development, or retain eggs in oviducts.
• Newts:
  • Internal fertilization with spermatophore in most.
  • Some primitive groups have external fertilization.
  • Eggs laid singly or in small groups.
  • Larvae similar to adults in morphology and diet.

Fertilization and Development in Frogs

• Frogs:
  • Vast majority with external fertilization.
  • A few exceptions are ovoviviparous.
  • Ascaphus with “tail”.
  • E. jasperi by cloacal opposition.
  • Full range of developmental options.
  • Where present, larvae very different from adults.
  • Undergo complete re-organization of body plan on metamorphosis.

Parental Care

• Any behavior by a parent towards its offspring that increases the offspring’s chances of survival.
• ICTHYOPHIDAE, PLETHODONTIDAE

A. Egg Attendance

• Usually by female, facultative, includes defense, cleaning, moistening.

B. Egg & Tadpole Carrying

• Both sexes but usually male, facultative and obligate.
• Gastrotheca marsupial frog (Female)
• Alytes obstetricians Midwife toad (Male)
• Associated with increased terrestriality, smaller clutches, and less frequent reproduction.

Energetic Cost of Parental Care

• The energetic cost may be substantial.
• Rheobatrachus silus - Southern Gastric Brooding Frog – Australia. Large, yolky eggs and tadpoles brooded in the stomach of the female.
• Rhinoderma spp. - Darwin’s Frogs – (Chile) Male carries late eggs / early tadpoles in vocal sac.

Extreme Parental Care: Caecilians

• e.g., Boulengerula taitana
  • Oviparous, direct development.
  • Female guards young.
  • Skin thickening.
  • Specialized teeth in young.
  • Feed on the skin of the female.
  • Multiple paternity, alloparental care.
  • Kupfer A., et al. 2006. Parental investment by skin feeding in a caecilian amphibian. Nature 440, 926-929.

Take-Home Messages

• Amphibians have evolved extremely varied reproductive strategies.
• Many instances of convergent evolution in different lineages.
• In all orders, there is a trend towards increasing terrestriality of reproductive mode, most pronounced in the anurans.
• Excellent model organisms for studies on the evolution of reproductive strategies.