According to paragraph 2, what allows some North American frog and toad species to survive in ambient temperatures well below freezing?
Their internal body temperatures never fall below -6ºC.
They do not remain at temperatures below freezing for very long periods of time.
Their tolerance boundaries are flexible.
Some of their body tissues contain substances that prevent freezing.
[#paragraph1]In contrast to mammals and birds, amphibians are unable to produce thermal energy through their metabolic activity, which would allow them to regulate their body temperature independent of the surrounding or ambient temperature. However, the idea that amphibians have no control whatsoever over their body temperature has been proven false because their body temperature does not always correspond to the surrounding temperature. While amphibians are poor thermoregulators, they do exercise control over their body temperature to a limited degree.
[#paragraph2]Physiological adaptations can assist amphibians in colonizing habitats where extreme conditions prevail. The tolerance range in body temperature represents the range of temperatures within which a species can survive. One species of North American newt is still active when temperatures drop to -2ºC while one [#highlight2]South American frog[/highlight2] feels comfortable even when temperatures rise to 41ºC—the highest body temperature measured in a free-ranging amphibian. [#insert1] Recently it has been shown that some North American frog and toad species can survive up to five days with a body temperature of -6ºC with approximately one-third of their body fluids frozen. [#insert2] The other tissues are protected because they contain the frost-protective agents glycerin or glucose. [#insert3] Additionally, in many species the tolerance boundaries are flexible and can change as a result of acclimatization (long-term exposure to particular conditions). [#insert4]
[#paragraph3]Frog species that remain exposed to the sun despite high diurnal (daytime) temperatures exhibit some fascinating modifications in the skin structure that function as morphological adaptations. Most amphibian skin is fully water permeable and is therefore not a barrier against evaporation or solar radiation. The African savanna frog Hyperolius viridiflavus stores guanine crystals in its skin, which enable it to better reflect solar radiation, thus providing protection against overheating. The tree frog [#highlight4]Phyllomedusa sauvagei[/highlight4] responds to evaporative losses with gland secretions that provide a greasy film over its entire body that helps prevent desiccation (dehydration).
[#paragraph4]However, behavior is by far the most important factor in thermoregulation. The principal elements in behavioral thermoregulation are basking (heliothermy), heat exchange with substrates such as rock or earth (thigmothermy), and diurnal and annual avoidance behaviors, which include moving to shelter during the day for cooling and hibernating or estivating (reducing activity during cold or hot weather, respectively). Heliothermy is especially common among frogs and toads: it allows them to increase their body temperature by more than 10ºC. The [#highlight6]Andean toad Bufo spinulosus[/highlight6] exposes itself immediately after sunrise on moist ground and [#highlight7]attains[/highlight7] its preferred body temperature by this means, long before either ground or air is correspondingly warmed. A positive side effect of [#highlight8]this approach[/highlight8] is that it accelerates the digestion of the prey consumed overnight, thus also accelerating growth. Thigmothermy is a behavior present in most amphibians, although pressing against the ground serves a dual purpose: heat absorption by conductivity and water absorption through the skin. The effect of thigmothermy is especially evident in the Andean toad during rainfall: its body temperature corresponds to the temperature of the warm earth and not to the much cooler air temperature.
[#paragraph5]Avoidance behavior occurs whenever physiological and morphological adaptations are insufficient to maintain body temperature within the vital range. Nocturnal activity in amphibians with low tolerance for high ambient temperatures is a typical thermoregulatory behavior of avoidance. Seasonal avoidance behavior is extremely important in many amphibians. Species whose habitat lies in the temperate latitudes are confronted by lethal low temperatures in winter, while species [#highlight10]dwelling[/highlight10] in arid and semi-arid regions are exposed to long dry, hot periods in summer.
[#paragraph6]In amphibians hibernation occurs in mud or deep holes away from frost. North of the Pyrenees Mountains, the natterjack toad offers a good example of hibernation, passing the winter dug deep into sandy ground. Conversely, natterjacks in southern Spain remain active during the mild winters common to the region and are instead forced into inactivity during the dry, hot summer season. Summer estivation also occurs by burrowing into the ground or hiding in cool, deep rock crevasses to avoid desiccation and lethal ambient temperatures. [#highlight12]Amphibians are therefore hardly at the mercy of ambient temperatures, since by means of the mechanisms described above they are more than able to exercise some control over their body temperature.[/highlight12]