Frogs. Early‑maturing or late‑maturing. Column in КомпьютерреOnline #55

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Dmytro Shabanov

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Toads. Early‑maturing and Late‑growing

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The thirteenth season has ended, during which my colleagues and I studied gray toads during their spawning. It seemed to me that some of our intermediate results might be of interest to the readers of KT. I will start from a distance and only at the end of the column will I move from particulars to general questions, okay? The gray toad is a solid terrestrial animal. It spends most of its life in forests. At twilight or on humid days it emerges from shelter, slowly patrols its area and gathers worms, slugs, beetles and woodlice. It overwinters in burrows under roots, and in spring, as the ground warms, it goes to spawn. This is where the most interesting part begins. Gray toads have an extremely developed philopatry – a tendency to return to the places where they developed as tadpoles for spawning. Cases have been described where, for several consecutive years, toads gathered on a parking lot at the site of an asphalted pond. Their relatively close relatives, green toads, also return to their spawning sites, but not as persistently. If a male green toad finds a suitable puddle, it stays, begins to sing its mating song – a bright, cheerful trill. The male’s throat resonator carries its voice across the area. The call of a single toad can be heard from several hundred meters, and a polyphonic chorus from two‑three kilometers. In such a situation females may go not to a familiar spawning site, but to the male’s call. Thanks to this plasticity, green toads easily colonize new habitats. Compared with them, gray toads are conservatives. This may be related to the fact that they spawn almost silently. At gray‑toad spawning sites only faint (they have no resonators) release cries are usually heard. For spawning, toads need to form pairs in which the male firmly holds the female under the armpits – this state is called amplexus. Oocyte maturation in the female is stimulated by contact with the male, which triggers the necessary hormonal signals. Thus, if a male gray toad grabs another male, the latter responds in one way, prompting release; a female with eggs responds differently, encouraging. Nevertheless, on some water bodies gray toads do sing quietly. How this population “style” influences the behavior of each individual is still not clear… I have written about gray‑toad spawning more than once. For the journal *Priroda* I wrote a piece on interspecific sex, and I posted photo‑reports on the breeding of gray toads that our working group conducts in the Iškiv pond near the biostation of our university on our website. Now I want to talk first and foremost about something else: the variants of strategy for structuring life. I will have to start with geography and history. In simplified terms, near my hometown, Kharkiv, there are two forest blocks. One, large, wraps around the city in a semicircle from the south and extends eastward to the border with Russia. The second, relatively isolated block is located north of the city, connecting with a forest‑park that the current authorities are gradually devouring piece by piece. Very roughly these two blocks are shown on the map.

[IMG_1] The southern block has always been inhabited by gray toads (well, within the observable time frame, of course). In the northern block conditions are very similar, but there were no toads there until the “wild ’90s”. Why? Toads thrive in a moderately anthropogenically altered landscape where forest patches and artificial water bodies coexist. Probably, several centuries ago the northern block lacked suitable water bodies. Later, suitable spawning sites appeared in the city’s vicinity, but a migration route from the southern block to the northern one was absent. Although they are close to each other west of the city, there were no appropriate water bodies; the territory turned out to be too altered. Thus, suitable habitats for toads “waited” there, which the toads could not colonize themselves. In other words, they could not do it. I helped. In 1994 I collected two bags of gray toads that had not spawned in the aforementioned Iškiv pond. I released the first bag into one of the suitable ponds in the northern block myself; my colleague delivered the second to another location. The next year I went to check the result. Not a single gray toad! I will say at once that artificial translocation of any animals is ethically questionable, and in some cases outright illegal. My case was not illegal, but was it ethical? In any case, I performed the act. I would like to believe that I have atoned for my sins before the toads… A few years passed. One spring I heard from an acquaintance how difficult it was to travel on the ring road north of the city. “The whole road is full of toads… which ones?” We went to look and saw ponds teeming with gray toads. Now I understand why I found none the year after the introduction. Adult toads that arrived at a new site did not return to it, because it did not become their home. But immediately after release the toads deposited some eggs. From them hatched tadpoles, which turned into juvenile toads and dispersed into the surrounding forests. For them those ponds became home, and, once grown, they returned to them. How do gray toads disperse on their own? We figured it out. I released toads into a downstream pond of a chain of three ponds. My colleague released toads into the upstream pond of a chain of seven. When we learned of the success of the introduction, all seven ponds populated from the top were already overflowing with toads. Tadpoles were carried from top to bottom by the water flow. In the area where I released them, the water, on the contrary, did not carry tadpoles into the neighboring water body. However, we were able to observe the first stages of colonization of the two ponds located higher up the stream. We arrived and saw two ponds separated by a dam and a distance of several dozen meters. I introduced toads into the lower one; they simply swarmed it. Spawning has just begun, and from the forested slopes where the ponds are situated, new toads keep descending onto them. For some of them the upper pond lies on the way. They climb into it, swim toward the lower pond, climb over the dam that separates the ponds and finally reach their small native habitat. Some females go alone; others have already met males and carry them on their backs. Lucky males trigger oocyte maturation. Rarely, a female may begin to spawn while still in the upper “transit” pond. Too bad she didn’t make it in time! Nevertheless, the tadpoles of this pair will imprint the new pond as their home. And if there is another water body nearby that they will have to cross as adults, they will eventually colonize it as well. Now I come to the main idea of my column. It did not come to us immediately. At first we simply noticed how large the females were in the newly colonized habitats and how small the males were. Look. The first photograph was taken in one of the new habitats. For toads, as for many other amphibians, females are generally larger, but the size disparity in this pair is excessively disproportionate. The female is very large, the male – tiny.

And the next photo was taken at the Iskovsky pond. The female is smaller, and the male (at least the upper one) is quite proportional in size. And behind him is another male, an intruder. He will have a difficult fight for the female.

[IMG_2] The next photograph was taken at the Iškiv pond. Here the female is smaller, and the male (at least the upper one) is fairly proportionate in size. In the background – another male, an intruder. He faces a tough battle for the female. [IMG_3] When measuring sufficiently large samples, it became clear that in “young” populations males are significantly smaller than in older ones, while females are, conversely, significantly larger (see Fig. 2 here). Now it is clear why, in habitats where toad density is consistently high, small males do not participate in spawning. It has been shown that a male’s chance of winning is proportional to his size (and thus his strength). The competition among them is serious.

[IMG_4] Where male competition is strong, a small male has almost no chance of fertilizing the clutch. Even if he encounters a female first, someone will still remove him from her. In contrast, where toads have only recently appeared and their population density is low, a small male may get lucky. If he meets a free female, he may simply avoid stronger competitors. Thus, we hypothesized why smaller males are found at spawning in “young” gray‑toad habitats. Why, then, do females grow larger there? Answering this requires precise data on growth rates, fecundity and lifespan of toads in the compared populations. I must tell you that obtaining reliable estimates of these crucial population characteristics for wild animals is a very labor‑intensive task. I will not rush events; data on age and growth rates of toads from the populations we studied have not yet been published. I will limit myself to a reference to general systemic patterns and mention our results obtained on frogs. General systemic considerations are based on the fact that a complex system with nonlinear internal interrelations cannot be optimized simultaneously for several different parameters. Here one can refer to the so‑called Matthew‑Kermak principle. Among biosystems drawn from a homogeneous set (e.g., organisms in a population) a high level of adaptation to one factor is linked to a low adaptation to others. This principle can be viewed as an example of a conservation law in biosystems. One can also speak of a trade‑off: the necessity to choose between optimizing parameters that are negatively correlated. It sounds complicated, but it reflects a quite accessible idea. Let me rather quote the best textbook on ecology, translated into Russian: “​It is easy to describe a hypothetical organism that possesses all the traits needed to achieve high reproductive value. It reproduces almost immediately after birth, produces numerous, large, protected offspring, cares for them; it reproduces repeatedly and often over a long life; it wins competitive battles, avoids predators and easily obtains food. Describing such a creature is easy, but imagining it is hard precisely because it is impossible to allocate all resources simultaneously to reproduction and to survival <…> Common sense already tells us that a real organism’s behavior and life cycle must reflect a compromise in the allocation of available resources.” Here, for me, the especially interesting thought is that a rapid shift to producing many offspring does not align with a long life; the priority in resource allocation may be linked either to reproduction or to survival. Now about frogs. In cross‑sections of tubular bones of frogs and toads, dark lines are preserved that form during hibernation. They vaguely resemble annual rings in tree trunks. Determining frog age, we found that the largest individuals are not the oldest, and the oldest are far from the largest. This is hard to reconcile with the widely known fact that both frogs and toads grow throughout life. We see it ourselves in bone sections! No matter how old a frog or toad becomes, it will continue to increase in size year after year, leaving evidence of this in its own bones. Here frogs are divided into two groups: “young” (in the fifth year of life) and “old” (older than six). Among the “young”, some grew quickly in the fourth year, some slowly. Almost all “old” individuals grew slowly in that same fourth year. Think about it: those that grew quickly did not survive to become “old”! Thus, among frogs there are fast‑growing (short‑lived) and long‑lived (but slow‑growing) individuals. These strategies can be named with terms used in fish farming and seed breeding – early‑maturing and late‑growing. However, these words should be understood not as two aspects of a single strategy (although sometimes they are used that way), but as designations of two alternatives. This is how I understand the situation. Late‑growing toads are optimized for a highly competitive environment. They grow slowly, mature late and spawn many times over their long lives. They maximize the number of offspring that can be produced over many years. Early‑maturing toads are adapted to a low‑competition environment. They grow quickly, mature early, but spawn only a few times because they live short lives. They maximize the number of offspring that can be produced in the near term. These two strategies differ from each other in the temporal horizon of “planning”! As for what follows from this and how it relates to our own lives – that will be for another time.

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Dmytro Shabanov

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Frogs. Early-maturing and slow-growing

Patient Strategy

Column in "KompyuterraOnline" No. 54

Column in "KompyuterraOnline" No. 55

Column in "KompyuterraOnline" No. 56