Were the Shai-Hulud fleeing even more terrifying SandVoles? I have never heard of worm grunting. This week I am going to ask some older folk about it.
In the Pines is one of my favorite songs! Also shown on Dirty Jobs! I used a spade fork to do that when I was a kid to get worms for bait. Mom appreciated me not digging holes all over the yard. We always called this fiddling for nightcrawlers. You cut down a small sapling in a damp area using a handsaw about a foot above the soil line. Then cut down the stump. The worms boil out of the soil by the hundreds. Pingback: Shock the Worm Root Simple.
Bars are SEM. Schematic illustration top view of the large, outdoor arena 1. Weather radar showing the relative rainfall for a thunderstorm on April 1st, , hours, during which observations of Diplocardia responses were made.
Observations were made during the first hour of rainfall for each trial rainfall was continuous and included periods of moderate and heavy rain. X marks the approximate location of the outdoor arena. Responses of earthworms in the large arena to a digging mole for 1 hour 5 trials and 1 hour of moderate to heavy rain 3 trials. See movies S3 and S4 for responses to digging moles.
The number of worms that emerged at different distances from the mole for 50 observations. Y-axis units represent worms per unit area as summed for the 50 trials and thus are arbitrary. Numbers for each square represent the raw total of worms for each distance. Summary of the directional preference for movement of the escaping worms for 30 observations.
The earthworms exhibited a marked response with a short latency—specifically, many worms rapidly exited to the soil surface and attempted to exit the area, often by crawling over the container walls.
A videotaped trial is included as movie S2. Earthworms seemed to have an escape response in the presence of moles. In this regard, it should be noted that eastern moles do not exit to the soil surface while foraging see discussion , thus fleeing to the surface provides worms both immediate safety and the most efficient means for movement away from the predator for subsequent burrowing.
In 5 trials, an average of In the different trials, the moles exhibited variable levels of activity, and each trial appeared to include relatively long periods of inactivity.
As a preliminary test for potential responses to rain and saturated soil, 50 worms were once again allowed to burrow into the soil for each of 5 boxes as described above. Each was then placed under a continuous sprinkler system that provided a simulated downpour at a rate of 1 inch per minute as measured by a rain gage. Each box was observed for 1 hour, and any worms that emerged were counted and removed. In 5 trials, 3 worms emerged from the soil in the containers during these trials Figure 5B.
As would be expected, by the end of the trials the soil was completely saturated and there was standing water on the soil surface of the containers. The soil was then removed from the containers and the earthworms were examined. In each case, the worms appeared healthy and had suffered no obvious deleterious effects.
Following these trials, 2 larger outdoor arenas measuring 1. Three hundred Diplocardia were then placed within each arena and allowed to burrow. After the earthworms had acclimated overnight, the containers were observed for 1 hour as a control period prior to the trial and any worms that had emerged before or during the 1 hour period were counted, removed, and replaced with new worms.
A mole was then placed on the soil surface, allowed to burrow, and the results were observed for one hour. These procedures were repeated for a total of 5 large-bin trials. The moles dug tunnels in various directions at different intervals, and this behavior and the corresponding surface ridges appeared indistinguishable from behavior and tunnels that were observed in the field see later section.
In response to the digging mole, many earthworms exited the soil and traveled across the surface movie S3. In these more natural trials, the potential utility of this response was more apparent, as the worms seemed clearly to be escaping from the digging mole. Many of the worms exited when the mole was quite close 5—10 cm but some worms exited at a distance of 20 centimeters or more e. In contrast to the behavior resulting from worm grunting, many of the earthworms appeared to have a directional response and moved away from the mole.
To document distance and direction of emergence more carefully, additional trials were performed with the camera in the same plane as the soil surface. Fifty earthworm escapes were filmed in this manner, and the distribution of distances from the mole to the emerging worm are shown in figure 5F. The direction of travel for the earthworms was also measured relative to the position of the mole for 30 trials Figure 5G. To examine potential responses to rain, the large arenas described above containing earthworms each were observed during thunderstorms accompanied by moderate to heavy rainfall, for a total of 3 large-bin trials.
The local weather radar for the period just prior to one of these trials am, April 1st, is illustrated in figure 5D , with the approximate location of the large arena indicated.
In the course of these three trials a total of 6 earthworms emerged to the soil surface. In each case, these few worms emerged after at least 25 minutes of steady rain. By the end of these trials, the soil was saturated and there was standing water on the soil surface the arenas had no drainage holes.
In the next 12—24 hours, depending on weather conditions, the soil was turned and the earthworms were examined and appeared healthy. Moles are powerful diggers that disturb the soil considerably as they use their forelimbs to extend tunnels and search for prey. Often, a mole digging in the wild is clearly audible to an observer standing several feet away see movie S5.
Sounds and corresponding ground vibrations are generated as the mole forcefully moves soil, scrapes its claws through the soil, and especially when networks of small roots ubiquitous in most of their habitat are broken. A number of geophone recordings were made as wild, foraging eastern moles extended their tunnels in Davidson County in Tennessee.
A 25 second example of these vibrations recorded with a vertically oriented geophone from a distance of approximately 15 cm is shown in figure 6A and see supplementary audio file S2. The peak amplitude of these vibrations was similar to the amplitude of vibrations caused by a worm grunter at a distance of approximately 6—10 meters Figure 1.
The frequency components power spectrum of a worm grunter and a digging mole are compared on a log scale in figure 6B. As might be expected, the worm grunter vibrations are more uniform, concentrated near 80 hz. The foraging mole produced a wider range of vibrations with the strongest peak near hz. Vertical geophone recording of a wild, foraging mole in Davidson county TN, from a distance of approximately 15 cm see supplementary audio file S2. Representative spectrums of a foraging mole from the first 23 seconds of the recording above and a worm grunter from the segment in figure 1C.
Recording of a single scratch from a foraging mole 1. This scratch was repeated multiple times 2 and then amplified over time 3 to simulate a digging mole. Arrow marks the point in the playback at which earthworms consistently emerged from the soil. Small arena used in playback experiments. Results of playback experiment. In 5 trials and average of 16 earthworms surfaced in response to the simulated mole. To examine how worms responded to vibrations caused by a digging mole, a section of a recording representing a single scratch Figure 6, C1 was copied into a new file and repeated at varied time intervals with silence between scratches Figure 6, C2.
This sound track was then amplified over time in an attempt to simulate an approaching mole for a 15 minute duration Figure 6, C3. These stimuli were then played through a speaker into the soil in the small arena containing 50 earthworms as previously described Figure 6D. In 5 trials, an average of 16 earthworms surfaced during the 1 hour time period movie S6.
In each case, the earthworms began to emerge during the 3 rd step of amplification. To obtain an approximate measure of the vibrations generated at this stage, a geophone was placed in the center of arena during playback.
The amplitude of the vibrations was similar to those obtained from a worm grunter at a distance of 8—10 meters. Although it was not possible to locate a wild mole actively extending its tunnel in the Apalachicola National Forest, such observations were possible in Davidson County Tennessee. This allowed for geophone recordings of naturally occurring foraging behavior, as previously described.
It also provided a striking example of earthworm escape responses occurring under natural conditions. In the course of roughly one hour of videotaped observations, more than 60 earthworms exited the soil near the burrowing mole see movie S5.
The mole could literally be tracked across the soil surface by the trail of escaping worms. In addition, 3 insect larvae exited the soil and traveled rapidly across the surface. The results of this investigation support the hypothesis that earthworms have a stereotyped escape response from foraging moles, and that bait collectors have unknowingly learned to mimic digging moles to flush worms.
The escape response consists of rapidly exiting the soil, which prevents pursuit by the mole, and allows efficient movement away from the mole for subsequent burrowing at a more distant location. The Apalachicola National Forest provided an ideal setting for this investigation for several reasons. First, there is a long history of bait collecting as a means of support for many families in and around the forest.
This suggests that earthworms in the area have a particularly strong response to vibrations and begs the question of why they should surface, exposing themselves to a host of terrestrial predators. Second, these bait collection practices continue to this day, allowing for observation and study of a technique that has been handed down for generations.
In this respect, I am indebted to Gary and Audrey Revell for their generosity in demonstrating how and where bait collection takes place, and for sharing their extensive knowledge of the forest ecosystems. This is not trivial, given that human introduction of earthworms across continents [12] , [13] has made such relationships difficult to access in many areas. The results raise a number of questions for further discussion and study.
For example, how widespread is this response among earthworm species and what other species might exhibit such escape behavior? How does this newly described response compare to other well-studied systems, such as echolocating bats and flying insects? What are the mechanisms and nervous system specializations that might account for the response?
What predators may exploit the longstanding predator-prey interactions between moles and earthworms and what other invertebrates may respond in this manner? These and other questions are discussed below. The results of this investigation, including observations within the National Forest, suggest that worm grunting does not simulate rainfall.
Evidence for this conclusion comes from the simulated rain experiments, during which few worms emerged, and the exposure of earthworms to thunderstorms with heavy rain, which produced similar results. In neither case did earthworms in saturated soil appear to be in distress.
In fact, more long-term observation of Diplocardia earthworms housed in outdoor arenas suggested the threat of desiccation was greater than that of drowning in a sudden downpour. Worms that remained in completely saturated soil for over 24 hours appeared in good health. In addition, no emerging worms were observed during one rainstorm within the Apalachicola National Forest personal observation. Finally, the behavior of Diplocardia during worm grunting does not seem an appropriate adaptation to avoiding drowning.
This impression comes from watching earthworms emerge in full daylight, during warm weather, onto hot, dry substrate. It seems unlikely that other strong sensory cues about moisture content in the environment would be over-ridden by vibrations, or that rapid emergence and movement in a random direction Figure 3D would be adaptive at the onset of rain e. Diplocardia do not move uphill in response to vibrations.
By contrast, the short latency of the response and rapid movement for an earthworm over the soil surface are appropriate for escaping a subterranean predator that does not surface to pursue prey personal observation, and see [14] , [15].
In this respect, the response is reminiscent of flying fish that can exit the water to travel briefly through the air where aquatic predators cannot follow [16]. For both prey items, the foray into the hostile environment is short-lived, but allows re-entry to the predator's realm at a more distant location. Why then are earthworms observed on the surface after heavy rains?
Perhaps the most obvious explanation is that a number of species of earthworms in different habitats are, in fact, potentially in danger of drowning after prolonged rainfall. For example, Chuang and Chen [17] recently examined oxygen consumption and surfacing behavior in 2 species of earthworms and found that one species Pontoscolex corethrurus had a lower rate of oxygen consumption and never emerged from the soil after heavy rain.
The other Amynthas gracilis had a higher rate of oxygen consumption and did surface after heavy rain. Thus some earthworms may be more sensitive to oxygen depletion in saturated soil [18] than others. But it is important to note that under conditions simulating heavy rain with saturated soil, the average time until A. This is consistent with the general observation that earthworms are often observed on the surface the morning after a heavy rain, but does not suggest these earthworms have a short-latency response to the onset of rain that might be cued by vibrations.
Dawkins [19] outlined this scenario, suggesting that a predator with a comparatively small impact on prey relative to more common predators may develop and maintain a strategy that exploits the prey's behavior - and by extension its nervous system [see also 20 for exploitive mimicry]. This has been well documented for painted redstarts Myioborus pictus that use high contrast plumage and tail fanning to elicit insect flight while foraging [21].
These flush-pursuit predators are thought to activate the hard-wired escape circuitry of insects [22] — [25] and may even direct the prey into the most sensitive part of their visual field for efficient pursuit. Evolution of this strategy depends on the predominance of gleaning predators, for which escape by flight remains the best insect defense [21].
Remarkably, humans are not the only ones to flush earthworms using vibrations. Tinbergen [4] noted that herring gulls exhibit a foot-paddling behavior, which flushes worms from the ground in Europe.
One is the bringing up of earthworms , which seem to have an innate reaction to the quivering of the soil which is of value , enabling them to escape their arch enemy , the mole. This presumably more common practice for gulls suggests the origins of the behavior, which might easily be transferred to the terrestrial setting where it could be subsequently reinforced through individual experience, selection over generations, or both.
Kaufmann documented a second example in wood turtles, which also stomp the ground to flush earthworms [5] , [26]. On over occasions wood turtles were observed to stomp the ground while foraging, and this behavior often elicited emergence of earthworms that were pursued and eaten.
Subsequent investigation revealed that others had independently observed the same behavior in wood turtles and the earthworm response [27]. Kaufmann was aware of bait collection techniques in the American southeast and specifically described the turtle's behavior as a form of worm grunting [28].
Like Tinbergen, Kaufmann attributed the earthworm's response to an escape behavior from moles. Apparently, the idea that earthworms respond to vibrations to avoid foraging moles has been considered for some time, but never formally tested. It may be that most biologists wondering about earthworm behavior have read Darwin's work on the subject [6] and noted his comments on the matter. However both Darwin and Tinbergen [4] make reference to unpublished personal communications from others.
This suggests that a number of naturalists have chanced upon a digging mole and noted escaping earthworms, as was observed in the present investigation. This in turn suggests such escape responses may be widespread for different earthworms responding to moles. The apparently widespread responses of earthworms to moles, and the ability of predators to exploit these responses, depend on the predominant selective pressure exerted by foraging moles.
What is the potential impact of moles on earthworms? Investigations of stomach contents of wild caught European moles Talpa europaea suggest they eat 60 g of food per day, with earthworms composing a large proportion of the diet [29] , [11]. This represents over 20 kg per year, more than half of which is usually earthworms [11].
Studies of the eastern mole Scalopus aquaticus suggest they may consume similar quantities of invertebrates, with earthworms making up a large proportion of the diet [30] , [31]. Our own experience with captive eastern moles, which we feed commercially available nightcrawlers Lumbricus , indicates they may easily consume their body weight in worms each day.
This was measured and confirmed for a single mole from the Apalachicola National Forest fed exclusively on Diplocardia earthworms collected by baiters. The 42 g mole consumed an average of 42 g of Diplocardia 23 per day over a 10 day period after 1 week of acclimation.
This likely represents more than would be eaten in the wild. Even so, half of this amount would be 7 kg of earthworms per year, or roughly 3—4 thousand adult Diplocardia 6—8 times the number shown in figure 2C.
Clearly moles represent an important potential predator of earthworms. The interaction between moles and earthworms is reminiscent of the sensory arms race between bats and flying insects [32] but is far less obvious due to the subterranean nature of the species involved it is also difficult to observe because moles, like earthworms, have their own predators and are themselves very sensitive to vibrations.
Bats are also small mammals that can have a strong impact on invertebrate populations. Although echolocation has provided a means for bats to exploit the night skies and the vast resource of flying insects, it also provides an obligatory and strong cue signaling insects of their approach.
Many diverse insects have developed bat-detecting ears and take evasive maneuvers in response to ultrasound. A number of moths exhibit a 2-tiered response, first changing course to fly away from the bat in response to low amplitude ultrasound, and then diving to the ground and acoustic crypsis in response to high amplitude ultrasound [32] , [33].
As is the case for bats, a mole digging a surface run in search of prey provides an inherent and potentially strong set of cues to prey as it approaches. Vibrations are an obvious component of these stimuli Figure 6A , and this was the focus of the present investigation in large part to explain the efficacy of worm grunting.
However, another potential cue was noted - that of local compression of the soil by the forelimbs during the power-stroke of digging. This lower frequency component was not obvious in geophone recordings, but could be imitated by briefly compressing the soil by hand. As was the case for vibrations, this stimulus also elicited escape responses from earthworms. This cue was not carefully investigated in the present study, in part for lack of a mechanism for producing controlled stimuli of sufficient force.
Yet it seems probable that escaping earthworms detect both vibrations as illustrated by worm-grunting and localized compression of the soil when escaping from a mole - the latter indicating a mole is particularly close. The combination of these two cues might elicit a more pronounced escape response than either presented alone.
The main technique is to drive a pitchfork into the ground, and rock it back and forth. This compresses the soil for a short distance around the pitchfork, and elicits escapes response from earthworms. Unlike the 80 hz vibrations produced during worm grunting that carry many meters, worm charming with a pitchfork appears to carry less than a meter, and thus has less dramatic results. The results raise a number of questions from the perspectives of ecology to neuroethology.
For example, it would be of interest to investigate how widespread these escape responses may be among the soil fauna, and what other predators might exploit such responses. It may also be that a large proportion of earthworms in the Apalachicola National Forest can escape mole predation by detecting their approach, requiring moles to depend on other invertebrates [e.
Moles in general are exquisitely sensitive to touch [35] , and it would be of interest to examine whether moles have developed counterstrategies. For example a mole that interposed itself between the soil surface and an earthworm could detect its relatively large burrow and trap it. What happens on the coldest winter days, when worms may be inactive but moles are active and in particular need of prey?
It may be that relocating territories in response to vibrations is essential for Diplocardia during warm weather, so that they are not vulnerable to predation during times of reduced activity.
Finally, the nervous system of earthworms in the genus Lumbricus is well known for the giant fibers that mediate the rapid withdrawal response [36] , [37]. Much has been learned about the electrophysiology of neurons and neuronal networks from such giant fiber systems, but it is often difficult to expand these physiological investigations to a natural setting.
Diplocaria might provide such an opportunity. Waypoints were downloaded into a Macintosh computer and imported into Google Earth. Distances between waypoints Figure 4C were plotted using the ruler function. To plot earthworm positions in the field Figure 3A , two Sonin Multi-Measure ultrasonic measuring units were used with receivers. The two receivers were placed several meters apart and measurements from each previously marked earthworm location were made to the nearest centimeter, one measurement to each receiver.
These measures provided a unique position plot for one side of the paired receivers for each marked earthworm. The distance between the receivers was used to plot 2 scaled position markers representing the receivers in an Adobe Illustrator document. For each marked receiver point, the circle command was then used to create a circle with radius equal to the scaled distance from each receiver to each earthworm mark.
The intersection of the 2 circles each centered on the receivers location represented the location of each marked earthworm, and these data are shown in figure 3A. To measure the shorter distances illustrated in Figure 3C , a tape measure was used in conjunction with a Strait-Line Model laser level with degree marks to measure the distance and angle of the earthworm locations relative to the stake.
The angle of the earthworm's path in relationship to the stake was measured with a segment of a folding wooden ruler, and then traced into a notebook.
These angles were later scanned and placed in Adobe Illustrator, measured to the nearest degree, and illustrated in Figure 3C. The angles traveled relative to the stake were used to compose the schematic in figure 3D see below for statistics. For distance measurements in large arena trials, a Cannon XL1 digital video camera was positioned in the same plane as the soil surface.
Videotapes of a reference scale were made in the same focal plane as the trials. Earthworm escapes from a foraging mole were then recorded, imported into Imovie version 6. Selected frames were exported from each trial and opened in Photoshop CS3 version The track of each earthworm and the location of the mole based on soil movements were then marked on the digital image while reviewing the video segment.
The mole's location was estimated as the central 4 cm of the soil disturbance at the time of earthworm escape—based on the consistent size of the mole tunnels.
This file was then placed in Adobe Illustrator where distances and angle of movement relative to the mole were measured. Department of Agriculture special use permit APA Moles from Davidson County Tennessee were collected under state permit number Moles were collected by observing the deflection of wooden dowels as the mole traveled through its tunnel system, blocking the mole's passage with hand trowels, and then removing the mole by hand. Diplocardia used in the mole-earthworm interactions were purchased from the Revells' bait shop.
Note that Diplocardia are not farmed and techniques for maintaining them long-term in an artificial natural setting have not been established. They are often maintained for bait in wood chips, but in this case they do not exhibit natural behaviors. To ensure healthy and active subjects, freshly collected specimens provided by the Revells were used for these investigations by arranging weekly deliveries.
All procedures were approved by the Vanderbilt Institutional Animal Care and Use Committee and are in accordance with the National Institutes of Health guidelines for the care and use of animals in research. Geophone recordings were made with Oyo Geospace geophones Houston, TX using a dedicated vertically or horizontally oriented model containing a GEO 11D transducer with a 4. The geophone output was through a coaxial cable that was connected to the audio input of a laptop without prior amplification or filtering.
All signals were recorded on a Macintosh G4 computer using Audacity software version 1. For the small arena trials comparing the control period, simulated rain, and a digging mole Figure 5B data were analyzed using a one-way ANOVA as an omnibus test for a main effect of condition. This was followed by post-hoc t -tests. The same procedure was used to compare the control period, rain, and a digging mole in the large outdoor arena Figure 5E. A t -test was used to compare the control period to playbacks of a digging mole Figure 6E.
Geophone recordings of worm grunting, as illustrated in figure 1C. This sound file plays amplified geophone recordings of a foraging mole as illustrated without amplification in figure 7A. It demonstrates some of the vibrations generated by moles as they forage. Gary and Audrey Revell demonstrate worm grunting to collect bait in the Apalachicola National Forest in Florida's panhandle. The Revell's are professional bait collectors and make their living by collecting the large earthworms native to the area.
These worms Diplocardia mississippiensis respond to vibrations by rapidly exiting their underground burrows. This is repeated in different areas until thousands of worms have been collected.
This video shows a preliminary test for earthworm responses to a burrowing mole. The container filled with dirt holds 50 Diplocardia earthworms. A mole is then introduced to the arena. As the mole digs, the earthworms exit to the surface and attempt to leave the area video is sped-up. In this video a mole burrows in the large arena filled with soil and containing Diplocardia earthworms. This shows a more natural setting and illustrates the pronounced escape responses sped up.
Because burrowing moles generally remain below ground while hunting worms, a worm that exits to the surface is safe from the hungry mole. Moles generate vibrations and soil compressions as they dig, and the results of this study suggest that worm grunters are simulating moles. This video is similar to video 3, showing a more natural setting and illustrating the pronounced escape responses sped up , but in this case showing some of the responses at longer distances form the mole.
In this video a wild, foraging mole extends its tunnel in Davidson County, Tennessee real time. Notice the sounds generated by the mole. These sounds are not rustling vegetation, but rather breaking roots as the mole forcefully pushes the soil upward.
This video shows earthworm escape responses to the amplified sound of a digging mole. The attached speaker is connected to a computer that is playing the recorded sound of a mole the recordings were made with a geophone. For an example of these recordings, listen to sound file B. Very special thanks to Gary and Audrey Revell. This study would not have been possible without their generous help and extensive knowledge of worm grunting, its history, and their willingness to share many insights about the ecology and geography of the Apalachicola National Forest.
Thanks also to David McCauley for suggesting the method of plotting positions in the field, and to Terry Page for advice on circular statistics. Conceived and designed the experiments: KCC. Performed the experiments: KCC. Analyzed the data: KCC. Wrote the paper: KCC. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract Background For generations many families in and around Florida's Apalachicola National Forest have supported themselves by collecting the large endemic earthworms Diplocardia mississippiensis.
Principal Findings Here it is shown that a population of eastern American moles Scalopus aquaticus inhabits the area where worms are collected and that earthworms have a pronounced escape response from moles consisting of rapidly exiting their burrows to flee across the soil surface. Conclusions Previous investigations have revealed that both wood turtles and herring gulls vibrate the ground to elicit earthworm escapes, indicating that a range of predators may exploit the predator-prey relationship between earthworms and moles.
Introduction In a number of parts of the southeastern United States, families have handed down traditional knowledge for collecting earthworms by vibrating the ground.
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