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Fear And Loathing in the Tropics Frogs Adapt to Survive

GAMBOA, Panama — The eyes of a caiman, an alligator-like reptile, reflect the beam of a flashlight shining on the pond, as, nearby, a snake slips through the shore undergrowth. Large spiders patrol the margins, and predacious water bugs skim the water's surface. It's a tough place to be a frog. But it's a great place to study fear and death.

That is exactly what Boston University associate professor Karen Warkentin—standing at water's edge wearing rubber boots and a headlamp—is doing. Along the way, she and her colleagues are challenging basic biological assumptions by illuminating the many different ways frogs develop in response to their environments.

It rained buckets earlier, and red-eyed tree frogs are calling enthusiastically. These slender frogs are to the tropics what loons are to New England—photogenic emblems of the wild. They are also fruitful research subjects. Warkentin has been studying them since 1991, when she staked out a pond in Costa Rica . The pond attracted many frogs and snakes, and she noticed two things: Frog eggs were not hatching at the same age, and snakes were eating a lot of the eggs.

After hundreds of hours of observation in the field and in the lab, she found that when a snake attacks a cluster of frog eggs, the vibrations prompt the embryos to hatch early. The eggs are mature at seven or eight days, but will hatch as early as five days in response to an attack. By hatching early, the embryos trade certain death by snake for the risk of being slightly underdeveloped and more vulnerable to predators when they splash down into the pond.

When Warkentin first presented her observations, many herpetologists harrumphed. But they came around after watching her videos of the attacks.

Warkentin says her research is part of a growing body of work showing how environmental influences affect development and survival. "It's not just what genes you have, but how you use them," said Warkentin. "Genes matter, the environment matters, and what you get in the end is dependent on both of them."

Since her initial discovery, she says, "I've kind of followed where these frogs have led me." That included a fellowship with the Smithsonian Tropical Research Institute, where she is a research associate. She spends at least two months a year at a Smithsonian field lab in an old school building in this Panama Canal town. Not only are there a number of well-studied frog ponds nearby, the institute excavated this pond for Warkentin four years ago, sculpted to her specs among trees at the edge of the jungle. The amphibians colonized it as soon as it held water.

Warkentin and her students have had some surprises.

Warkentin and Justin Touchon, a doctoral candidate at BU, found that tadpoles raised in tanks with fish develop clear, slender tails, while those in tanks with dragonfly larvae develop big red tails. The adaptations allow them to better escape the different predators.

"What it shows is that these animals are much more complex than we think," said Touchon.

Touchon also found that hourglass tree frogs, which usually lay eggs on leaves over water, instead laying their eggs in the water—marking the first time that a vertebrate has been known to lay eggs both on land and in the water, a sort of evolutionary bridge species.

In one experiment, Touchon moved frogs that were about to lay eggs to enclosures with water-filled kiddie pools and overhanging plants. Half the enclosures were in an open field, where eggs laid on leaves would be at risk of drying up in the hot daytime temperatures, the other half were in the shade nearby. Although neither group of frogs had ever seen their new habitat in daylight, the vast majority of each group laid their eggs in the place best suited to the daytime conditions—in the cooling water for those in the sun, on the leaves for those in the shade.

"The idea that frogs make these really smart decisions about where to lay their eggs surprises most people," said Touchon. His photo of these frogs made the cover of the Proceedings of the National Academies of Science, which published his paper in May.

Warkentin has found complexity at every turn. Not only can red-eyed tree frogs hatch early to escape predators, they can also complete their metamorphosis and leave ponds early to escape tadpole predators such as water bugs, or delay metamorphosis when there's an abundance of pond-side predators such as fishing spiders. Fear of predators, it turns out, strongly influences not just frog behavior but also physical development.

Warkentin is also investigating early development, growth within the egg, and how eggs hatch.

But her biggest project is nicknamed "fear and death." It occupies a large field near the experimental pond. Each of the 200 tanks that hold 100 gallons is stocked with tadpoles. Some tanks have no predators, some have dragonfly larvae, and some have water bugs. In some tanks the predators are loose among the prey, in others they are suspended in nets where they are fed tadpoles but can't prey on the general population. The tadpoles detect the predators' presence through chemical signals.

Warkentin hopes this project will provide answers to a big question: In a frog's world, "what's the relative importance of fear and death?"

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