Little Loggers Make a Big Difference
|It could be that the old fields that resist tree invasion for decades are those in which the vole populations are chronically high.
Voles are common denizens of virtually every habitat (other than dry desert) in the temperate, boreal, and arctic zones of the Northern Hemisphere. Of the roughly 120 species of voles worldwide, about a dozen are notorious for their boom-and-bust population fluctuations; one of these is the meadow vole. But unlike the populations of some of their more famous relatives (more famous to ecologists, at least), whose population fluctuations follow a regular, three-year cycle, some meadow vole populations irrupt sporadically and others almost always stay high or low. Biologists interested in the radical population swings of voles and their close relatives, the lemmings, have focused almost exclusively on why such fluctuations occur rather than on what the wider impact is. Hearing of the devastation of the researchers experimental tree seedlings by marauding rodents, my plant ecologist colleague Charles Canham and I decided to investigate whether the fluctuations in vole populations might be important in determining when and whether tree seedlings are able to invade old fields: we wondered whether trees can establish themselves only when the voles go bust. If so, it could be that the old fields that resist tree invasion for decades are those in which the vole populations are chronically high, and those that get overgrown quickly are able to do so because their vole populations crash frequently.
Canham and I established nine enclosures in a grassy field on the grounds of the Institute of Ecosystem Studies in Millbrook, New York. We chose a typical northeastern hayfieldhabitat thats wonderful for voles but also likely to get rapidly overgrown if left unmown. The enclosures were each about a third of an acre, and wire-mesh fencing more than three feet high kept all but the most intrepid voles from moving between them. For two years we kept track of the populations every other week by livetrapping and marking each individual with a numbered ear tag. Within each enclosure, we kept the vole population at one of three density levels: about 400, 175, and 80 voles per hectare. We chose such distinct levels to match what happens naturally. To maintain these vole densities over the course of the experiment, we had to keep removing individuals from the lower-density enclosures. (We released these animals in another field about a mile away. Some voles, we learned, can navigate their way home from this distanceeven wading through streams, crossing paved roads, and scaling fences to get there.)
Inside the enclosures we planted small seedlings of several tree species that commonly colonize old fields in the eastern United States, Quebec, and Ontario, and we monitored their fates for up to a year. In that time, the densest vole populations eliminated about 95 percent of seedlings, whereas medium- and low-density populations killed about 80 and 65 percent, respectively. The voles, it turned out, preferred red maple, white ash, and tree-of-heaven seedlings and turned up their noses at those of white pine and red oak. Such high levels of destruction, combined with such clear food preferences, suggest that these animals control the species composition of regrowing forests.
Seedlings killed by voles are easy to identify: the stems are clipped near ground level, leaving tiny, diagonally cut stumps. We were puzzled to find that about a third of the clippings went uneaten and were left to rot. Were the voles not searching for food but instead managing their habitat by keeping woody plants from invading the grassy fields that voles prefer? After all, other animals appear to engineer their environment for their own future benefitbeavers create wet meadows by damming streams, elephants aid grasses by destroying savanna trees. But individual beavers and elephants live long enough to benefit from the work, so the evolutionary rewards plausibly outweigh the costs. A vole lives no more than a year, and it is hard to imagine an individual vole reaping much benefit from killing a several-inch-tall seedling that is years away from shading out grasses and eliminating vole habitat. Only if the voles descendants, several generations later, lived in the same area could there be an evolutionary benefit from clipping seedlings, and the propensity of the voles offspring to disperse makes that unlikely. Perhaps, we speculated, voles constantly explore potential new foods, and the few surviving seedlings belonged to species that proved bad tasting.
|We knew that various hawks, owls, snakes, and mammals prey on the voles and that these rodents have a number of adaptations to compensate for their popularity as food.
If noxious taste might protect seedlings, what else would have the same effect? Canham and I tried our best to think like meadow voles. We knew that various hawks, owls, snakes, and mammals prey on the voles and that these rodents have a number of adaptations to compensate for their popularity as food. One is reproductivefemales reach sexual maturity at three to four weeks of age and become sexually receptive within a day of giving birth. One litter of approximately four to five young is suckled while the next brood is gestating. Other adaptations include selecting safe haunts and being discreet. Its easy for vole aficionados to impress the uninitiated by predicting which spots in a field are best for finding voles: simply parting the tallest, densest patches of grass will more than likely reveal vole feces, as well as small piles of grass clippings characteristic of vole activity and narrow runways. In shorter, sparser vegetation or near the bare dirt around woodchuck or gopher mounds, such signs will be rare. Canham and I planted seedlings down the middle of small clearings that were intended to simulate woodchuck mounds or other disturbances; in keeping with our expectations, the voles almost never touched these seedlings, even when their populations were quite dense. Lingering in the open, it seems, is not worth the risk of being killed by a sharp-eyed predator, especially an aerial one.
Tall grass is no perfect refuge, however. Mammalian carnivores such as weasels and foxes catch voles by chasing or pouncing and are probably just as dangerous in dense cover as in sparse. Perhaps, I thought, mammalian predators indirectly protect tree seedlings in all habitatsnot just in clearingsby trimming the vole populations or at least scaring them into inactivity. My colleague Jyrki Pusenius and I got the idea of tricking the voles into perceiving that they were in danger. We created an audiotape with the sounds of a weasel calling and a weasel catching a vole. With speakers wired to a van parked on the study site, we played the tape every night for two weeks inside some of the enclosures while we monitored the fate of seedlings. To our amazement, voles clipped more seedlings in enclosures where they heard taped weasel sounds than in those where no tapes were played. The same thing happened when we placed a caged weasel inside one enclosure. And neither the feces of bobcats nor the urine of foxes, coyotes, and bobcats discouraged voles from attacking seedlings. The smells of these predators had no more effect than the odor of dilute vinegar. Only when these carnivores actually eat voles do they become accidental allies of the little trees.
Most of the trees that invade old fields have fairly large seeds that dont fall far from the parent plant. Even maple and ash seeds, with their helicopter-like samaras, may float only a few dozen yards on the wind, while larger seeds, such as acorns, beechnuts, and hickory nuts, drop like stones. (Exceptions do exist: tiny, winged aspen and birch seeds may float thousands of yards, and cherry and red cedar seeds are swallowed by fruit-eating birds and defecated at some distant spot.) Because of this modest dispersal distance, the invasion of old fields by trees usually proceeds most rapidly near forest edges, where the influx of seeds can be tremendous. Several colleagues and I therefore decided to establish our next generation of experiments at the boundary between forests and fields. Two students, Robert Manson and Jaclyn Schnurr, had already demonstrated that the ubiquitous white-footed mouse is a seed predator extraordinaire, and we thought that mice and voles might provide a one-two punch that could undermine tree colonization of old fields. While meadow voles rarely leave grassy fields to enter forests, white-footed mice are generalists, preferring forests but frequenting old fields as well.
|It makes sense that, as seedling predators,
voles have a greater impact on tree regeneration than do seed-eating mice.
This time, our enclosures extended five and a half yards into the forest and thirty-eight yards into the field. Each enclosure had three walls and was open on the forest side. We suspected that the voles would treat the forest edge like a fourth wall but that the mice would freely enter the old fields. Again we created vole populations of differing density levels. As before, attack rates on tree seedlings correlated well with vole density. However, we found that wherever vole density was high, mouse density was low, and wherever we kept voles scarce, mice thrived. We dont know exactly how voles deter mice, but we suspect that voles, which are twice the size of mice and about ten times as pugnacious, may attack and chase any mice they encounter. Whatever the mechanism, the result was that enclosures with a high vole density had low seedling survival but high seed survival, whereas those with a low vole density had good seedling but poor seed survival.
A crucial twist is that not only do voles eat seedlings while mice eat seeds, but voles and mice have different food preferences. Mice avoid the smaller and less protein-rich seeds of maples, ashes, and trees-of-heaven but devour the larger, more nutritious seeds of pines and oaks. Pines and oaks, then, should invade old fields dominated by voles (assuming that parent trees reside somewhere nearby), and maples and ashes should colonize old fields dominated by mice. But since few, if any, long-term records are available to tell us which types of old fields each animal inhabits, testing this expectation is difficult.
However, because we maintained the high and low vole population levels within our three-walled enclosures for about four years, we were able to observe which species of rodent had the stronger net impact on tree invasion. Manson surveyed all the experimental plots and found very few naturally occurring seedlings where voles were abundant and mice were scarce. On the other hand, many more natural seedlings flourished where voles were kept rare and mice were plentiful. It makes sense that, as seedling predators, voles have a greater impact on tree regeneration than do seed-eating mice. Any individual forest tree can produce tens of thousands of seeds (or more) in any given autumn, and even if the mice consume 95 percent of those seeds, a healthy number of seedlings could survive. On the other hand, after everything else that may kill seedsfungi, bacteria, insects, birds, mice, infertilityhas had its way, far fewer seedlings than seeds will be present. So a dense vole population that kills almost every tree seedling can strongly inhibit the regrowth of forests.
The life of the meadow vole has wider implications than I suspected the first time my cat bestowed upon me a small, brown, and very dead one. Its targeting of seedlings has prompted some utilities, as an alternative to using herbicides or machinery to control trees, to look into making their power-line corridors favorable to voles. These rodents also play a strong role in preserving attractive vistas and maintaining the open habitats favored by such other wildlife as deer, turkeys, woodcocks, and bluebirds. And meadow voles, by excluding white-footed mice from some habitats, may reduce the risk of Lyme disease, which is carried by ticks that feed off (and are infected by) these mice. Nearly omnipresent, these voracious killers of tree seedlings might even affect the global climate by delaying or preventing the expansion of woods at a time when the absorption of carbon would be very helpful. All these wider implications are nearly invisibleuntil you push back the tall grass and have a look.
Copyright © 2002 American Museum of Natural History