Shabanov (2011) Grey toads, green frogs: love and death in cold water

Shabanov D. A. Grey toads, green frogs: love and death in cold water // Nature. – 2011. – No. 4 (1148). – pp. 56–59. Grey toads, green frogs: love and death in cold water Shabanov D. A.  Year after year, after the spring warmth consumes the winter reserves of snow and ice, a captivating event unfolds in lakes and puddles, rivers and ponds. The breeding of amphibians. The species that, like grey toads, overwinter on land awaken when warmth penetrates the moist soil and the roots of trees. The amphibians that, like lake frogs, overwinter on the bottom of water bodies awaken with the melting of the ice cover, with changes in the temperature and gas regime of the bottom water. The current year is the twelfth in which we and our colleagues have observed the breeding of grey toads at the Iškiv pond near the biological station of Kharkiv University. Since 2000 we have annually marked toads that come to breed (in some years more than a thousand individuals) and have recorded encounters with already “familiar” individuals. Remarkably, until 2010 we encountered toads marked in 2000. For a toad’s lifespan this is a great many. Will we meet them in 2011? It will become clear when this journal goes out of print. Why do we mark them? We are trying to determine the factors that govern the developmental strategy of toads. What determines what portion of energy a grey toad will allocate to its own growth and what portion to offspring production? In our view, the ratio of these expenditures may be influenced by the conditions of tadpole development, in particular the intensity of competition among conspecifics. During our observations not only the population size of toads at Iškiv pond changed, but also the growth rates of individual specimens. Notable results have already been obtained, but no one intends to stop the observations. Each subsequent year turns out to be more interesting than the previous one… But that is a topic for another story. The purpose of this article is to describe the traps into which the sexual instinct drives tailless amphibians. Thus, our tailless amphibians— toads, frogs, garlic frogs, tree frogs, and newts— have external fertilization. The majority of the species breeding in Iškiv pond overwinter on land. Males and females move to the breeding site independently. It is important that the female deposits eggs, protected by swelling mucous membranes, in the presence of a male. In the absence of a partner, all energy spent on egg production would be wasted. To avoid untimely egg laying, tailless amphibians have evolved a particular behavior—amplexus (from Latin amplexus— to embrace, to encircle). Upon finding a female, the male tightly embraces her with his forelimbs and… thereby stimulates egg maturation. He may even help the female during spawning, extruding the eggs—portion after portion. [IMG_1] Amplexus of grey toads. The pair can remain in this position for more than a day, which is required for egg maturation in the female Photo A.V. Korshunova Think it’s easy to hold a slippery female in cold water? To prevent her from slipping away, the male during amplexus presses his forelimbs hard against her sides; on the inner surface of these limbs are the breeding pads—velvety‑rough areas of swollen skin. During spawning the breeding pads darken, but even outside the breeding period they stand out against adjacent skin. These patches can be used to distinguish females from males. However, in the case of grey toads it is usually unnecessary to examine the limbs: males of this species are smaller than females and differ in shape. The female’s body is expanded posteriorly by the egg reserves. [IMG_2] Breeding pads on the male’s feet, allowing him to hold the female during amplexus Photo D.D. Korolesova In grey toads males arrive at water bodies earlier than females. In fact, the female does not have to rush—she will always be in time for her spawning. The male is in a different situation—he may be late and end up without a female. Hence the males hurry. They arrive at the water first and wait at the water’s edge—in spots suitable for egg laying. If a male is lucky enough to meet a female still on land, he will take her in amplexus, and she will have to carry him on her back. Obviously, the male who finds a female before the others gains an advantage. Therefore, when females are scarce, males become extremely indiscriminate. They are ready to lunge at any moving object that, by size, somewhat resembles a female. When waves move objects floating on the water surface, male grey toads may be attracted to last year’s reed shoot or even a dead fish. Objects that move on their own are especially attractive. Fortunately, the attention of male grey toads is most often captured by their conspecifics. [IMG_3] A lucky male: he will reach the water body on a female Photo A.V. Korshunova When one toad tries to take another into amplexus, the latter emits a characteristic release cry: if it is a male, the sound resembles a sob; if it is a female—a whimper. The typical male response leads the aggressor to lose interest, while the female’s response (especially if she has not yet released her batch of eggs) makes the male tighten his grip even more. When many males are present, they try to grab each other in amplexus, but always break free and emit a characteristic “male” release cry. As a result, a group of captured breeding males produces sounds reminiscent of a chick or duckling brood chirping. Which female is attractive to a male? A large one. If she is truly large, she can attract an entire group of males. Is it good to be the object of such heightened interest? Increased competition among males will result in her offspring being fertilized by the most successful sperm donor. [IMG_4] Probably not easy for her: the female’s head between the heads of competing males Photo A.V. Korshunova Male‑male collisions can be serious. If a solitary male encounters a pair in amplexus, he may try to wedge himself between the partners and thereby break their bond. The male holding the female drives the competitor away, attempting to push him with his legs. In such contests, the larger and stronger males ultimately prevail. [IMG_5] A usurper may try to break up the formed pair on land… Photo A.V. Korshunova [IMG_6] …and in water. The outcome of the fight depends not only on luck but also on the strength and agility of the males Photo D.A. Shabanov The same water bodies are used by different amphibian species. The breeding at Iškiv pond is started by grey toads and sharp‑snouted frogs. At the same time, common garlic frogs, red‑belly newts, common tree frogs, as well as newts—common and crested—join them. The breeding of green frogs does not begin yet. Green frogs are not a single species but a group of two parental species (lake and pond) and their hybrid—the edible frog. Lake frogs overwinter on the bottom of water bodies and may emerge from hibernation precisely during the grey toads’ breeding. Over time, edible frogs that overwintered on land will also appear, while there are no pond frogs in Iškiv pond. Green frogs, as well as green toads, will begin breeding later, when the water warms. In summer all these amphibians disperse to their permanent habitats and will practically not compete with each other. However, their larvae have to develop in the same pond. Tadpoles of newts differ in their lifestyle—they are predators that swallow small aquatic animals. Tadpoles of all frog species in Iškiv pond feed by scraping a variety of plant and animal material from wherever it is available. This may include plant and animal encrustations on submerged objects, aquatic plants, and sometimes even animals (a dead frog, for example). Despite dietary specialization, the food spectrum of tadpoles of different species overlaps, making them competitors. Thus, during breeding different amphibian species are found together, and it is not surprising that male tailless amphibians, which can be attracted by a waving reed shoot or a dead fish, also respond to their more or less distant relatives. Consequently, in water bodies with a diverse amphibian fauna (batrachofauna) heterospecific amplexuses are formed. We have observed a sharp‑snouted frog male taking a garlic frog in amplexus, and a garlic frog male taking a crested newt male! In fact, all amphibians are poisonous. Each species produces a characteristic set of toxins intended both for suppressing bacteria and for combating potential predators and competitors. Typically, each species is resistant to its own toxins and sensitive to the chemical weapons of other species. What happens during close physical contact of individuals of two species? After a while each feels ill from the foreign toxins, and the “incorrect” amplexus disintegrates without serious consequences. [IMG_7] Top—male sharp‑snouted frog in a blue breeding dress; bottom—garlic frog (note the vertical pupil) Photo A.V. Korshunova [IMG_8] And the male crested newt is certainly not involved: tailed amphibians have internal fertilization. Unfortunately, the male garlic frog has a strong grip Photo A.V. Korshunova [IMG_9] It is clear how such a heterospecific amplexus will end: the sharp‑snouted frog male will feel sick from the grey toad’s toxin and will release his hold Photo A.V. Korshunova From the described pattern there is one important exception. If spring is early, lake frogs emerging from hibernation have a high chance of encountering solitary male grey toads on the shores. This leads to a heterospecific amplexus in which grey toads hold lake frogs. Several males may pile onto a large lake‑frog female. Such amplexuses often end only with the frog’s death. [IMG_10] Grey toad holding a green frog in amplexus Photo A.V. Korshunova [IMG_11] This lake frog turned out to be larger and therefore more attractive Photo A.V. Korshunova Toads are fairly resistant to frog toxins. Conversely, it is known that toad venom is most effective against other ectotherms, and frogs (potential competitors of toads at the larval stage) are more sensitive to it than mammals and birds (potential predators). Look into the eyes of the frog held by a male toad. She is already under deep anesthesia. We will not include photographs showing how the frog’s body swells under the grip of grey toads, how the strong limbs of male toads tear inflamed frog skin… After those days when such encounters occur, dead frog bodies lie on the shores, killed by toads. [IMG_12] The lake‑frog female’s eyes are hidden by a cloudy film; the grey‑toad male, apparently, is full of enthusiasm Photo A.V. Korshunova How to classify such an interaction? It is a very peculiar form of interference competition, i.e., competition accompanied by direct interaction between competing species. As you have understood, this variant is based on the deviant sexual behavior of grey toads. By the way, interference competition is usually an adaptation that reduces the intensity of exploitative competition—interactions in which competitors diminish each other’s access to jointly exploitable resources. If frog and toad tadpoles compete with each other, such male toad behavior can indeed be favored by selection. Of course, trying to understand what goes on in a toad’s mind is a futile endeavor. Yet, judging by all external manifestations, during the chemical killing of a frog the male toad runs the same behavioral programs as during a normal amplexus in which he embraces a female of his own species. Indeed, love and death are constantly intertwined!