Goo-eating snakes and the eggs that evade them

One tradition at WCH meetings is to open each day with a plenary talk, which is an hour-long presentation by a distinguished herpetologist. Of the several plenaries at WCH7, the one that impressed me the most was given on the first day by Karen Warkentin, a herpetologist at Boston University who studies environmentally-cued hatching of amphibian eggs. One of the foundations of her research is that the timing of hatching, a critical life-stage transition in the life of an amphibian (or reptile), should be flexible in order to maximize the likelihood of survival of the young animals. That is, if the egg is safe from predators and pathogens, hatching should be delayed as long as possible (typically until the embryo is as large as it can get without leaving the egg). However, if the egg is in danger, hatching should speed up, as long as the embryo is capable of living outside of the egg. This phenomenon is observed in a variety of reptiles and amphibians, including  the Agalychnis (red-eyed) treefrogs that Dr. Warkentin studies. These frogs lay their eggs on leaves overhanging pools in the Neotropical rain forests, so that when they hatch the tadpoles can drop into the water.

The primary predators of Agalychnis eggs are wasps and snakes. In the wild, snakes consume as much as 50% of all Agalychnis eggs laid, so it makes sense that there would be strong selection for eggs that could escape snake predation. If a snake or wasp attacks a clutch of eggs, the vibrations trigger the eggs to hatch almost immediately. If that sounds impossible, check out this video of a Parrotsnake (Leptophis) attacking a clutch of eggs:

Look at those little guys hatch! You can see other videos at Dr. Warkentin's website, where you can compare the feeding behavior of Leptophis with that of the Cat-eyed Snake (Leptodeira). Embryos in the last third of their development escape from snake attacks with about an 80% success rate by hatching up to 30% early, which is really remarkable. Furthermore, they can distinguish snake attacks from other sources of vibration, so that they don't hatch every time it rains. To do this, they respond to several non-redundant vibrational cues, including frequency, duration, and their interaction. These cues propagate throughout the jelly matrix of the eggs, so that eggs that have not yet been touched by the snake can escape. In two species of Agalychnis that have reduced jelly, escape success is much lower, because the signals do not propagate as well.

According to Dr. Warkentin, the snakes do not appear to prefer younger eggs (which would be incapable of hatching early) or to forage preferentially in the rain (when their vibrations might be masked by raindrops). Along with Leptophis and Leptodeira, two other snake genera, Sibon and Dipsas, possess morphological and behavioral adaptations for feeding on frog eggs and other prey items that are essentially 'goo'. Not unlike the southeast Asian pareatids I've covered before, these Neotropical snakes have numerous, long, slender teeth on the dentary (lower jaw), and they have many skeletal and muscular modifications that allow for jaw flexibility beyond even that normally seen in snakes. Extinction of many frogs due to chytrid fungus in Central America has caused dietary shifts and changes in abundance of these snakes.

Environmentally-cued hatching in response to vibrations also occurs in the eggs of other treefrogs, centrolenid glass frogs, and African reed frogs. It can also occur in response to other environmental dangers, such as flooding (in salamander and some turtle eggs) and disease (in frog eggs and also in painted turtle hatchlings, which often overwinter in the nest but are more likely to emerge early when infected with sarcophagid fly larvae). This last example comes from the thesis work of Julia Riley at Laurentian University, who presented preliminary results at the WCH. She also found that turtles hatching in nests that were on steeper slopes were more likely to emerge early, possibly to avoid collapse of the nest over the winter. Whether research will one day show that snake eggs also possess environmentally-cued hatching plasticity is an open question, but I suggest that a good system to start looking would be the Nicrophorus beetle hosts. Maybe we'll be hearing about that at WCH8 in Hangzhou, China!

ACKNOWLEDGMENTS

Thanks to Otto Monge, Brad Wilson, and the Warkentin lab website for providing photos and videos.

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