Summer World: A Season of Bounty - Bernd Heinrich (2009)
Chapter 3. Wood Frogs
28 May 2006. IT RAINED FOR A WEEK AND NO INSECTS flew. But today the sun came out and I heard the first gray tree frogs. One male was calling from a branch above the road as I jogged by, and I stopped to find him. He was a gorgeous green (not grayish as suggested by the name). After I climbed up, got him, and brought him home, I put him in a terrarium for a detailed look. He perched on a twig and stayed there like an ornament, but continued to call in three-or four-minute bouts at approximately hourly intervals. When at rest he has a deflated throat that vibrates rapidly at very low amplitude. Then, to call, his whole plump body contracts and suddenly looks skinny, while his loud penetrating churring sound erupts at the same time that his throat balloon inflates.
He produces his loud penetrating calls by exhaling to inflate his throat balloon, and his abdominal contraction is the engine for that burst of sound. With that penetrating sound, his whole body vibrates to its frequency. When my (temporary) pet called, several others within 100 yards of our house joined in. The females, like most other frogs, presumably go toward the loudest, generally nearest, individuals they hear. What a stark contrast to wood frogs that I had watched the month before!
Fig. 6. Male tree frog calling and advertising himself.
IF ANIMALS’ MAIN SUMMER PREOCCUPATION IS A RACE of reproduction, then the chorus of wood frogs on a night in early April is the starting gun. The frogs burst out from under the decaying leaves on the ground, overnight meet at a pool that has just melted, and start their convocation, which is rowdy, loud, and brief. One might assume that the males call to attract females specifically to themselves, but now, after getting to know them a little better, I think the story of what they do is more interesting. As we shall see, it can involve cannibalism, and more.
For about eight months the wood frogs crouch, with their heads down and their limbs tucked tightly to their sides, under the leaves that settle on the ground in the fall, and they and the leaves are then covered with snow. The frogs often freeze solid, and in that condition they don’t have a heartbeat, breathing, digestion, or activity of the brain cells. A reputable human pathologist, applying the same clinical standards to them as he would to one of us, would conclude that they are dead.
The wood frogs’ cue to revive and arise as from the dead, like that of the alder, hazel, and poplar flower buds, usually comes on the first warm (40°F) rainy day in April. By the millions freshly thawed frogs crawl out from under the cool damp leaves, and each of them starts hopping in a beeline to a little pool somewhere in the woods. They arrive at it from all directions. The whole population in any one area will travel mostly at night, and most of the frogs arrive on only one particular night. But adjacent pools are not necessarily on exactly the same schedule. Traffic to a pool on these nights can be intense; up to 4,000 frogs have been counted coming to a single pool in three hours (Bevan 1981).
All fall, winter, and spring the frogs had fasted and waited for their cues to arise and become active. During thaws in January or February, the aboveground temperatures on occasion rose to nearly 60°F, but the frogs still did not budge. Even after they do become active, they still do not feed for some time. First things first. For wood frogs that means sex and egg laying, which they accomplish simultaneously.
Fig. 7. A male wood frog in calling position on a pool.
I wrote in my diary entry for 14 April 1995 that I had arrived at about ten o’clock the night before at camp in Maine, driving in a drizzle and being impressed by the “traffic.” The main traffic on my trip from Vermont that night happened to be crossing the road, and it was mostly wood frogs. While coming through New Hampshire I saw them as pebble-like lumps in my headlights against the black, wet tarmac. At one point I was induced to stop my pickup truck, and I caught twenty of them, both males and females. Every one of them had been facing or hopping toward where I could hear a male chorus at full throttle. The road was also littered with the flattened dead—those who had previously attempted to join the gathering throng. From a distance a wood frog congregation sounds like a gaggle of peripatetic ducks. Presumably it is irresistible to female frogs, and I suspect it is to the males as well.
Fig. 8. Part of an aggregation of male wood frogs on a pool.
Although the wood frog choruses in different pools are often on their own schedules several days apart, group chorusing is not entirely due to similar arrival times of the participants in any one pool. Getting there on the same night makes it possible to sing together, but that alone does not ensure a chorus. Only the males call, and not at random with respect to one another. Already timed to arrive at the pool within about a day or two, the individuals further synchronize their calling with each other.
The wood frogs’ chorusing is, like that of most frogs, an energetically extreme exertion. In their case it’s done on a stomach that has been empty since fall. But that exertion is only a prelude for the wrestling matches that commence almost immediately among the males in their attempt to capture females who come to the pool at about the same time. For most of the males that make it to a pool, the first day they get there will be the only one in their lives to mate. Even then, less than 40 percent of them will get that chance. On the other hand, of the females that make it (at outcome about six times less likely for the females than the males), virtually all will have a mate within seconds of hopping into the pool. Each lucky male who does get a female wraps his forearms around her and locks his thumbs together under her neck.
Fig. 9. Male wood frog with neck lock on a female, who will swim with him to the spawning place.
It is almost impossible for one male to pry another off, and the males stay attached to their prospective mates for hours and potentially days (if one were to remove them from the pool). A female, even if she is dead, can have a dozen suitors attached to her on various appendages and in various positions. Half a dozen or more males may simultaneously try to lock onto a single live female, but only one of them will achieve the one sure position—a solid neck lock as he perches on her back. He won’t let go, and the resulting twosome may look like a two-headed, four-legged mutation; at least one such coupled pair was claimed as such, by a woman who excitedly brought it to my office.
The female then takes the locked-on male for a ride. She swims to the one spot in the pool where all the other frogs will also deposit their eggs. He will not release her until she has laid her walnut-size lump of several hundred eggs, and he then releases his sperm onto them and also releases his grip around her neck. She will then almost immediately leave the pool. This is probably the last time in their lives that either will ever have contact with open water again, except for those rare and lucky individuals who manage to survive another year. If they do survive, then they unerringly return to the same pool they left the year before. Much has been found out and there is still much to ponder about these fascinating animals, but several questions jumped into my mind.
Where and Why Do Wood Frogs “Nest” Communally?
Much about the unique behavior of wood frogs, whose breeding and larval life are strictly dependent on water, can probably be understood from the standpoint of a highly evolved lifestyle that is suited for breeding in temporary pools—those that are subject to drying out early in the summer. As many as twenty frogs spawned in a tire-track depression behind our house, and this depression usually dried out even before the eggs hatched. However, the frogs have no prescience of how long the water in any pool will last. Thousands of them breed in a beaver pond along our road. A year after the beavers made it, this pond was populated by frogs. On the other hand, another beaver pond near our house has never attracted a wood frog chorus in the twenty-five years that I have been watching and listening. It is, however, an ancient (i.e., “permanent”) pond, one that is populated not only by all the other local frog species, but—more significantly for the wood frogs—also by minnows, sunfish, and catfish. Wood frogs even breed every year in a washtub-size pool formed in a rock depression on a hill at my camp in Maine. This particular pool is not subject to dropping groundwater levels, and I’ve never seen it dry out, but fish have never reached it. In short, wood frogs avoid breeding in water that contains fish; and the smaller the pool, the more likely it is to dry out at some time during the summer and therefore to be fishless. Pool size, permanence, and impermanence, as such, make no difference. Apparently, adult wood frogs have an aversion to fish, and for good reason. Wood frog tadpoles have the bad habit (relative to other frog tadpoles) of swimming around conspicuously near the water surface and feeding there on algae, rather than hiding on the bottom like most other tadpoles. I released a handful of wood frog tadpoles into an aquarium containing native fish that immediately went into a feeding frenzy and ate every single one.
It may seem odd that although the frogs don’t care much about size, and perhaps other physical attributes of a pool or pond in which they spawn, they nevertheless are very particular about where in the pool they spawn. The females make an effort to deposit their eggs at the same place where others have already done so. The males are also nearby, gathered for their chorus. But you need a large pond to notice this. Three miles down the road from our house is a pond about 660 feet long and 165 feet wide. It has ample space for frogs to spread out, yet every spring the wood frog chorus is restricted to an area of several square yards on one end, and almost all the many females drop their eggs there, in one big pile. Why?
Although an individual egg clump is only walnut-size when deposited, it swells to the size of a baseball or softball within hours because the gelatin surrounding each egg absorbs water. When hundreds of individual egg clumps are deposited next to each other, there is a solid expanse of jelly densely dotted with the black eggs (they are white on the bottom, and they right themselves if turned). For female frogs it presumably feels right to swim to where others have spawned or will spawn. We might say that they respond to a “social releaser.” And for a male, the releaser to release his sperm is probably the female’s releases of her eggs. The frogs do not know the connection between their acts and the ultimate or evolutionary sense or consequences of these acts. Nor do they need to.
It seemed to me that the wood frogs’ egg aggregation might have something to do with elevating egg temperature to speed up hatching rate. Using my electronic thermometer, which I had then been using mainly to measure the body temperature of bees, I immediately got busy, waded into the icy waters of many pools, and measured the temperatures around the edges. I found no evidence that egg clumps are located in warmer parts of the pools relative to other parts, so the frogs did not search for or find any hot spots in their pools. But temperature could still be important in egg placement.
The upper black surfaces of wood frog eggs must absorb heat in sunlight, but the heat would normally be quickly dissipated by convection to the cooler water around them. However, a large mass of jelly embedding the eggs would reduce water movement and could aid heat retention. The larger the effective mass, the less heat loss from the center. So, to find out if there is a measurable effect, I took dozens of egg clump temperatures versus surrounding water temperature, and compared single and clumped egg clusters. The results: Egg clusters in shade are nearly the same temperature as that of the water surrounding them. However, in sunshine, the single egg masses were heated on average 3.5°F above the surrounding water temperature, and clusters of ten or more egg masses were heated 9 to 13°F above water temperature.
Temperature affects the developmental rate of the eggs. To find out how much, I brought egg clumps into the lab to determine the time until they hatched. In the woodland pools I had measured egg mass temperatures of 43°F to 79°F, and in the lab none of the eggs hatched that were held either below 41°F or above 86°F. In between these extremes, the developmental rate of embryos was directly related to temperature. For example, eggs at 46°F required thirteen days to hatch, and eggs at 68°F hatched in six days. Thus, within the physiologically suitable temperature range, every increase of 3°F in egg temperature speeds up the hatching date by a day. That could be a huge potential advantage, since the snow-melt pools that these frogs use are highly ephemeral in the summer.
After finishing my temperature measurements I was both pleasantly surprised and also a little disappointed to learn that I had indeed been on the right track. Egg clumping for heating was an idea that had already been proposed. Bruce Waldman from Cornell University had published a detailed study a decade earlier, where he found that the edges of wood frog egg masses were heated several degrees above water temperature while the centers warmed to over five F higher.
Why Do the Wood Frogs Call?
If there is one tenet that I knew beforehand to be firmly established in the scientific literature on frogs and toads, it is that males compete in attracting mates by making conspicuous vocal displays, and that females choose. Like the singing by birds and many insects, most famously crickets, katydids, and cicadas, the calling by frogs is an advertisement in which a male draws attention to himself or to some resources he holds that females need for reproduction. I know of no published exception to this explanation for male frogs’ mating calls. Biologists agree that calling sets up competition among males, allowing females to sort them out and choose. If several calling males are near each other, they can presumably be all the more easily compared, so that females can exercise even better choice. Indeed, aggregations of males where females come to be mated are considered the equivalent of mate marts where the males strut their stuff (if they can, or if they have enough to be allowed by the competition, or both). The females generally choose a small number of individuals out of the participants. Do wood frogs? My hunch was that they do not. And this time I consulted the literature as well as the frogs.
Three research papers on wood frogs’ mating aggregations appeared between 1980 and 1985. The first one, by Richard D. Howard (1980), then at the University of Michigan, established that the males outnumber the females at the breeding pools by about six to one. The skewed sex ratio apparently results from different mortality; fewer females live long enough to reproduce because it takes them one year longer than the males to become sexually mature. Each female was found to pair with only one male, and vice versa—a condition that is, I think ironically, described as “monogamy.” There is an intense competitive scramble among the males, but Howard was unable to demonstrate any choice by females. A nearly simultaneous study by Keith A. Bervan (1981) also reported no evidence for female choice. Bervan also found that any female would be clasped long before she reached any calling male that she might choose. The males don’t have the luxury to choose, either. Bervan noted that they attempt to clasp with each other, with any females, and even with already firmly clasped pairs. That is, males cast a wide net, try to capture a mate first, and discriminate later; those males on the receiving end of a “trial embrace” give a call that identifies their gender, and they are then immediately released. However, they are not so easily deterred from females who already have a male attached to them. If the female doesn’t make a quick enough getaway after she has a male, she will quickly accumulate a surplus of males that restrict her mobility. The other males try to grasp her around the abdomen and then move upward in an attempt to pry the other male off her back. They rarely succeed, but they can do so if the competing male is small enough and the female is so large that her male can’t reach all the way around her neck to secure a solid lock with his thumbs.
If these two studies weren’t enough to dispel the notion or expectation of female choice in wood frogs, another one did. This next study, by Richard D. Howard and Arnold G. Kluge of the University of Michigan (1985), emphatically concurs with the previous studies. These authors write, confidently: “Our results were unambiguous: the slightest movement by females resulted in their immediate amplexus [locking on of male] by the nearest male.” And females did not dislodge those potentially unwanted males; only other males did that, in athletic wrestling contests where size and strength mattered. Thus the most exhaustive and broadest study of “mate choice” yet (involving reams of data on survivorship, growth rates, numerical estimates of zygotes produced by females and sired by males, and monitoring of 5,877 individually identified frogs) still had found no evidence of mate choice in wood frogs. My hunch, derived from one glance into a pool, had apparently been right, but hunches as such seldom win kudos.
It may seem that there was little left to learn about the mating habits of wood frogs, given the solid empirical results. However, I still wondered: If females don’t choose, then why do males call at all? What could they call for?
To answer this, or any other relevant biological question, it helps to look first at the context in the field, in the animals’ natural environment. Wood frogs are unlike any of the other species of local frogs in that wood frog males are not spread out. By contrast, male tree frogs are separated from each other by trees; spring peepers, green frogs, bullfrogs, and other pond breeders are usually scattered along a shoreline or over an expanse of marsh where they can be hidden in little niches under leaves and grass that allow them to control space around themselves. Calling wood frog males are easily visible, massed on open water near the center of their little pool.
Several days after I had seen the wood frogs crossing the road at night while I was driving to Maine, I sat down near the edge of a pool near my camp. This pool, which is no larger than the floor space of an average room, contained at least fifty highly visible male frogs. They were spread out, as is typical, about a foot apart all over the surface of the pool, with only the tops of their heads out of the water while their hind legs trailed behind. They floated in place and occasionally paddled with alternate strokes of their hind legs. They approached any other frog they came near. I saw only one female jump into the pool. At least I assumed it was a female, because only this one was pounced on almost instantly and not released. In seconds, three males were on top of her, and one of them got a tight neck lock. It was, as always in wood frogs, a classic competitive scramble with the males in an intense contest for the females, who are literally up for grabs.
In one ball of ten squirming males that I untangled I found a dead female at the center. I threw her back into the pool, and she was again mobbed and embraced in the same way. I suspect that there were so many males on this dead female because she could not escape. But males’ preference could also be involved, because males “should” prefer more rotund females: such females would make the males’ sometimes prolonged wrestling efforts more worthwhile, since they would get more eggs with one shot (so to speak). My dead female happened to be rotund indeed—she was bloated with gas, though, instead of eggs. In any case, she could not have chosen any of these males; they all chose her. Whatever the calling behavior of one or the other of these amorous males, it had made no difference to this particular long-dead female. However, an anthropomorphism readily suggests itself to describe what might be going on. Is the frogs’ chorus a collective effort of the males to get females to come into their pool, like guys at a Saturday night college fraternity party playing loud music to attract the most babes to go to their house as opposed to a neighboring one?
At first I watched the frogs from a distance of about twenty feet, so as not to disturb their activities. Their calling was, as usual, in concert; some of the time the whole crowd seemed to be sounding off, and then there were periods of silence, as though the band played all together for most effect, then took an occasional break before resuming with renewed vigor. After a while, one or two of the frogs started up again, the rest then joined in, and their voices blended in. (By contrast, with many other frogs and toads one can easily pick out individuals by differences in pitch.) I had brought along a tape player to record the chorus. I reversed the tape and played back their calls during a silent period after I had disturbed them and they had dived to the bottom. Almost instantly after I turned on the sound, frogs started popping up to the surface and chimed in with the taped sound. I then shut the sound off, and then they stopped too. When I again played the tape I got the same result. I repeated the trial fifteen times, and it always worked.
Like most summer activities, the frogs’ vocal signaling requires an impressive expenditure of energy (Taigen and Wells 1985) and therefore presumably has an advantage. However, it is not immediately obvious why the calling of an individual wood frog in a chorus could aid him snag a female that has jumped into the pool. If not, then why call at all, as long as other nearby males are doing all the work and bringing females in by their calling? Instead of having a mating advantage, calling would seem to be disadvantageous, because the noncallers, who save their energy, should have an advantage in the inevitable tussling contests that ensue among the males seconds after a female jumps into their crowd. In the extensive literature on the mating game there are indeed innumerable examples of “satellite” males (those that wait to intercept females coming to the displaying males they are attracted to), who adopt the energetically more economical mating strategy. So, why don’t they all stay silent? And after one frog called, then all the satellites should especially be silent. Instead, all the neighbors joined in. It didn’t seem to make sense from the perspective of satellite males. But I knew it makes sense—somehow.
Although the frogs’ synchronous chorusing in crowds was puzzling to me, someone thoroughly steeped in frog literature would not have been confused. One reviewer commented about an article I had submitted that was summarily rejected: “Why of course they would chime in. Frogs do that. When your competitor is calling you had better immediately call as well to remain in the picture as far as a potential mate is concerned.” This idea makes intuitive sense, of course, but only in terms of females’ choice. I had regularly observed exactly that—in other frogs, those that are hidden and widely spaced, such as gray tree frogs, spring peepers, green frogs, and maybe bullfrogs (although those in our pond also aggregated to produce deafening pulses of sound where hundreds joined in, separated by moments of absolute silence). Why should male wood frogs chime in with the chorus of voices when there is no way for an attentive female to choose specific preferred individuals out of the chorus line? I didn’t know. But I didn’t think they were performing like the participants in a summer music festival. Or were they?
In a scenario of an intense, proximate, competitive male-male scramble for females, the idea that frogs could be “cooperating” for anything is not intuitive. But as an example of possible ultimate cooperation at the same time, suppose a frog’s voice reaches one mile. Then the area of a circle with a radius of 1 mile is pi (about 3.14) times 1 mile squared, or about 3.14 square miles. Suppose further that there is one female in this area, and that the calling male frog could on average attract only one female. Then if ten frogs start calling synchronously from that same spot, and their combined volume rather than the individuals’ volume as such counts, the combined vocal volume (pi × 10 squared) is now increased tenfold and would sweep about 314 square miles of area, reaching an audience of 100 females. That is, the ten frogs who call synchronously to amplify the attractant could expect to increase the number of females attracted up to a hundredfold, while their interindividual competition increased only tenfold. Per individual, then, each achieves a tenfold advantage by joining in the communal chorus.
How to Describe the Young Frogs’ Summer Race?
Regardless of ultimate cooperation by males in attracting mates, northern wood frogs breeding in woodland puddles live on the edge of survival and proximally compete for their lives. In their ephemeral pools, wood frogs have only about two months of summer to complete their larval development. Often they run out of time. In 1995, twenty-one of the twenty-four pools I was watching were dry by the beginning of July. (The next two years brought the wettest springs on record in Vermont, and none of the pools dried out.) In 1999 all my pools were dry by May 18; it was one of the driest springs on record. But as I will show, cannibalism then saved some froglet cohorts from annihilation.
After getting the earliest possible start following the spring melt, the next step in the wood frog’s race with time is to get the tadpoles developed into frogs and hence out of the pool before it dries up. This step mainly involves the development of the larvae; they must grow fast, or be able to act like adults (hop on the ground; breathe air), or both. Two main ingredients make the difference in this race: food availability and temperature. Any increase in body temperature above the near-freezing water temperature that the tadpoles find themselves in permits an increase in growth rate, and they must simultaneously have access to sufficient amounts of the right kinds of food, particularly protein.
Wood frog tadpoles are primarily vegetarian. They feed on algae. But algae are not their only food. When I kept tadpoles indoors in an aquarium, adding nothing but a few decaying leaves picked out of woodland pools, they fed on these leaves and skeletonized them so that only a fine latticework of leaf veins remained. Larvae fed on dead leaves were still alive at the end of February, when I found them under the ice of a rain barrel where I had dumped eggs the previous April. Apparently an insufficient (low-protein) diet can extend the tadpoles’ life span from several weeks to at least ten months. Conversely, when I fed them some “fish flakes,” a high-protein commercial aquarium diet, they had a growth spurt.
Freshly metamorphosed froglets look and act like adults. However, they weigh as little as 0.007 ounce (0.2 gram), about one-hundredth of the adults’ mass. The specific size of the tadpole where evolution has set the developmental switch to produce the adult form is flexible, but in wood frogs it has presumably been strongly influenced by time. The smaller the tadpole at the set point, the shorter the time to get there. Still, in many years the larvae run out of time and don’t make it to the froglet stage. When I checked on one of my biggest study pools on 11 June 1999, I found the center a moist black goo of dead and dying wood frog tadpoles. It was surrounded by the tracks of raccoons and great blue herons. Carrion beetles and maggots were mopping up the edges. Similar scenes were repeated at other wood frog breeding pools, but as I found out later, this did not mean the wood frogs’ breeding at those pools was necessarily a failure that year.
I scooped up a few spoonfuls of the dead and dying wood frog tadpoles and dumped them into my aquarium with their living relatives. The larvae immediately consumed the dead and weakened of their own kind, and literally overnight they grew hind legs. The next day they added front legs as well, and the following day their tails shrank. They still swam like tadpoles when in the water, but they hopped like frogs the minute they were on land. In three days the change to a cannibalistic diet had caused them to become frogs, whereas the other larvae of the same batch who were maintained on decaying leaves were still tadpoles seven or eight months later. I suspect therefore that as the pools dry up in the summer, feeding frenzies on their own kind impel some froglets to life on land.
Initially a pool where no more than 100 females have deposited their clutches of 300 to 1,000 eggs each may contain at least 50,000 tadpoles. Collectively they represent the nutrients that have been concentrated from highly dispersed and often microscopic food particles by the collective grazing of the tadpoles over the span of a month or two. They become a nutrient store that could later give their brethren a boost to lift them out of the pool as the water disappears. If the same scenario is repeated regularly through evolutionary time, then cannibalism could be an important part of this frog’s survival “strategy” (a response resulting from evolutionary selection).
Temporary pools are a prime component of the wood frogs’ summer world, and I conclude that almost everything they do is highly evolved to take advantage of it. Their specific behavioral mechanisms blur the meaning of, or give new meaning to, our ideas of “cooperation” and “competition.”