Anuran Reproductive Modes: Evolving Perspectives
Although most of the unique ways that frogs reproduce were described in the 1800s and 1900s, additional modes are still being discovered in the 21st Century. The concept of reproductive mode has evolved from descriptive natural history to an integration of developmental biology, genetics, systematics, evolution, ecology, behavior, and physiology that frames our thinking about the transition of vertebrates from water to land and about anuran reproductive adaptations to diverse environments today. We have classified reproductive modes, examined quantitative parameters, searched for geographical and ecological patterns, and described variability. We have speculated about selective pressures guiding the evolution of terrestrial reproduction and argued about the usefulness of reproductive mode as a character to construct phylogenies. In the past, researchers assumed that the reproductive modes exhibited by living frogs represented stages in an incomplete, linear sequence of steps toward greater independence from open water, with direct development at the end of the spectrum. Newly proposed phylogenies based on molecular data allow us to re-think the evolution of anuran reproductive modes. On another level, we are increasingly realizing the value of incorporating life history information (aquatic larvae or terrestrial development) in setting priorities to formulate more effective and ecologically relevant conservation strategies. The next decade is certain to witness significant advances in our understanding of anuran reproductive modes.Abstract
Eggs of representatives of the three main groups of reproductive modes: A = Dermatonotus muelleri (eggs deposited in water, aquatic larvae); B = Dendropsophus bokermanni (eggs deposited out of water, aquatic larvae); C = Craugastor sp. (eggs deposited out of water, no aquatic larval stage—in Craugastor, direct development). Photos by Martha Crump.
Nests of two foam nest-breeding species: A = Pleurodema borelli (Rufous Four-eyed Frog; eggs abandoned after deposition); B = Leptodactylus latrans (Criolla Frog; female stays in center of foam nest and guards clutch against potential predators). Photo A by Martha Crump; B by Célio Haddad.
Male Hypsiboas faber (Blacksmith Treefrog) guarding eggs floating on water surface in constructed nest. Photo by Célio Haddad.
In Aplastodiscus leucopygius (Guinle Treefrog) eggs are deposited in a constructed subterranean chamber: A = entrance to subterranean chamber; B = unpigmented eggs floating on water in chamber. Photos by Célio Haddad.
Eggs of Chiasmocleis leucosticta (Santa Catarina Humming Frog) floating on water surface in bubble nest. Photo by Célio Haddad.
The ancestral reproductive mode is presumed to be eggs and exotrophic tadpoles that develop in open water. Pictured here is a new genus and species of pipid from Minas Gerais, Brazil, around 30 million years old, which likely exhibited this reproductive mode. A = tadpole; B = metamorphosing young; C = adult. Photos by Célio Haddad, who is currently describing the fossils.
Examples of parental care: A = female Pipa carvalhoi (Carvalho's Surinam Toad) with eggs embedded in dorsum; B = female Fritziana sp. (undescribed species) carrying eggs in dorsal pouch; C = male Phyllobates terribilis (Golden Poison Frog) transporting tadpoles; D = male Rhinoderma darwinii (Darwin's Frog) brooding tadpoles in vocal sac. Photos A and B by Célio Haddad; C by Danté Fenolio; D by Martha Crump.
Leptodactylus bufonius (Mud-nesting Frog) an example of a reproductive mode with terrestrial eggs and aquatic larvae. Males construct mud nests on the ground in low-lying areas and call from inside the nests. Amplectant pairs produce foam nests inside the mud nests, and the females cap the nest openings with mud. Following heavy rains, the nests break open and exotrophic tadpoles are washed out into the newly-formed ponds where they complete development. A = newly-constructed mud nest; B = capped mud nest with foam nest inside. Photos by Martha Crump.
Phasmahyla cochranae (Chocolatefoot Leaf Frog) an example of a reproductive mode with terrestrial eggs and aquatic larvae. Eggs are deposited on leaves above fast-flowing streams. After hatching, the exotrophic tadpoles fall into the water below where they complete development. Empty capsules among the eggs provide moisture, and the folded leaf further protects the eggs from desiccation. A = folded leaf containing egg clutch; B = opened leaf exposing eggs. Photos by Célio Haddad.
