by Kenneth Christiansen
ABOUT THIS ISSUE
Published by Emporia State University
Prepared and issued by the Division of Biological Sciences
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Cover Figure: Three typical unspecialized springtails of the families: Hypogastruridae, Entomobryidae, and Sminthuridae (top to bottom).
Other Kansas School Naturalists on related topics:
"Insects" KSN Vol. 10, No. 2 (out-of-print, photocopy available for $1.00)
"Bees" KSN Vol. 16, No. 1 (out-of-print, photocopy available for $1.00)
"Tiger Hunting in Kansas" KSN Vol. 19, No. 2 (FREE)
"I Didn't Know That! Insects" KSN Vol. 25, No. 4 (FREE)
"Making An Insect Collection" KSN Vol. 35, No. 1 (out-of-print, photocopy available for $1.00)
"Scientific Names, Common Names" KSN Vol. 37, No. 1 (photocopy available for $1.00)
"Checklist of Kansas Butterflies" KSN Vol. 37, No. 4 (color, available for $1.00)
"Snow Flies" KSN Vol. 38, No. 2 (FREE)
Caring for Creatures in the Classroom
K.U. Museum of Natural History, Lawrence, KS 66045-2454; Registration deadline November 5; fee: $35.00.
This workshop is designed to help teachers feel more comfortable with animal visitors in their classrooms. Choosing appropriate animals and how to care for them will be emphasized. We will discuss common wild and domesticated animals, from slugs and snakes to frogs and ferrets. Included will be demonstrations, handouts, guest speakers, and of course, guest critters. For more information, contact the K.U. Museum of Natural History, Office of Public Education, (913) 864-4173.
Due to a funding shortage, the next issue of the Kansas School Naturalist is anticipated in 1993.
The printing and distribution of this issue of the Kansas School Naturalist is partly underwritten by grants from the Ross Foundation and the Price R. and Flora A. Reid Foundation, both of Wichita, Kansas, and by contributions from readers like you.
ABOUT THE AUTHOR
Dr. Kenneth Christiansen is Professor Emeritus of Biology at Grinnell College, Iowa, and one of a few remaining authorities on the Collembola, or springtails.
by Kenneth Christiansen
You probably have had the experience of seeing a small black speck go scurrying across a sheet of paper and suddenly disappear. IF you have ever had house plants you have probably at sometime seen large numbers of tiny white creatures crawling around under or on flower pots. You may have walked through the woods on a sunny day when the snow was still on the ground and seen some dark blue patches on the snow. If you looked at these patches more closely, you discovered they consisted of thousands of tiny insect-like creatures called "snowfleas." If you have spent time at the seashore at low tide, you may have noticed small tide pools or wet rocks with tiny blue-black animals covering the surface. Few people realize that in all these cases these motile motes were springtails or Collembola. Although Collembola are among the most numerous arthropods on earth's surface, and over four thousand different species are recognized, they are little known,a and those who are aware of their existence generally think of them either as "snow fleas" or as soil insects. This is understandable, since Collembola are almost all tiny (mostly less than 3 millimeters long) and are most conspicuous when they emerge in vast numbers on snow on a warm winter day, and since they are one of the most important elements in any soil ecosystem. However, Collembola are not limited to these situations, but occur almost everywhere from the tops of the tallest trees to the deepest soil strata where life occurs. They are in fact found everywhere life of any sort is found except the open ocean or below surface in bodies of freshwater.
For example, the black speck on the paper is one of number of household springtails which have become part of man's arthropod entourage. In North America the most common representative of this group is Willowsia nigromaculata (Figure 1) and the animated comma racing over your page was very probably a member of this species.
A good many species of Collembola thrive in the soil litter or fallen logs and sticks where they feed primarily on fungi and bacteria. Under ideal conditions, often in eh winter when predators are scarce, they may build up huge numbers under the snow. A warm sunny day may increase the level of activity so much that they appear to boil out onto the snow surface. Although a number of species can do this, occurrences in the United States usually involve the common snow flea, Hypogastrura nivicola (Figure 2). Some people become worried by the vast numbers of snow fleas and their sudden appearance on the ground. But there is no cause for alarm; they are totally harmless to us and our plants, houses, or animals. The best control measure is to wait a day and they will be gone. A few will make it back into the soil but most will die, shrivel up and blow away.
Most Collembola prefer cool, damp environments. Very few can tolerate house climate for long or even those conditions under which most crops are grown. Thus, they are unlikely to compete with the cockroach or the medfly for public attention. Another man-made habitats which better suit their requirements, they may be exceedingly common. Certain species swarm in beds of cultivated mushrooms or earthworm cultures; these and others may be conspicuous inhabitants of greenhouses, or thrive amid ornamental plants in flowerpots. Many such springtails are white or very pale; the species you found on or under your flowerpots was probably Folsomia candida (Figure 3) which lacks eyes as well as pigment.
Many species of Collembola can only live in the intertidal zone at the seashore. During high tide they hide under stones, in rock crevices or any other place, enclosed in air droplets formed as their water repellent cuticle contacts the water. During low tide they come out to feed. If you saw specimens on the east coast of the United States or in Europe, they were probably members of the genus Anurida (Figure 4) since these are among the most abundant sea shore Collembola. Because they lack the ability to move on water, they are frequently temporarily trapped on small tide pools. Many other species occur in the same habitat or in the interstitial space in shoreline or littoral sand. This unique habitat, formed in the shore line sand where the freshwater seeping down form land meets the salt water seeping in from the ocean, is inhabited by many species of Collembola. The fact that most of these species are restricted to this zone suggests a high degree of physiological specialization.
Springtails are all wingless arthropods which, similar to insects, have six legs but are not closely related to them. Even the unspecialized types show a variety of body shapes and three basic unspecialized types are shown on the cover. While Collembola vary greatly in most features, all are wingless and the primitive forms generally have most of the characteristic features shown in Figure 5. One of the most remarkable of these is the peculiar jumping apparatus, called the furcula, near the end of the abdomen. It is this structure which gives Collembola their common name of "Springtails." This structure is normally kept tucked under the body, held in place by a sort of latch mechanism called the tenaculum.When the latch is released, the furcula snaps back with great force, driving the animal up to 100 times its body length. This usually allows the animal to escape any attacker, but there is a problem. The Collembolan has absolutely no control over which way it goes or where it is going to come down. Imagine that you are jumping the height of a two story house and up to a half a block in distance but have no control over where you will land! Fortunately Collembola are probably not given to anxiety attacks. Many specialized types of Collembola such as the Anurida (Figure 4) have, through evolution, lost the furcula and all jumping ability with it.
An even more unusual feature is the ventral tube. This structure is present on all Collembola and in no other animals. Its bottom is always wet and usually sticky and this in some forms allows the animals to stick to any smooth or wet surface, even when upside down. Its thin wet surface also serves as a respiratory organ since Collembola generally lack any other specialized organs for this purpose and largely obtain oxygen through their thin cuticle or skin. Probably the most important function of the ventral tube is drinking. A very tiny capillary tube is drinking. A very tiny capillary tube runs from the bottom of the ventral tube to the mouth and when the animals which to drink, they stick the tube into a drop of water and suck the water off the tope of this tube - sort of like carrying your own soda-straw with you everywhere.
Springtails are more or less well covered by simple to very complicated hairs or setae of many sorts and, in some groups, scales. A variety of these setae is shown in Figure 6. In addition some groups have heavy spines; when they occur at the end of the abdomen they are called anal horns (see in Figure 5).
The heads of Collembola are always oval and they have four antenna segments. In specialized forms these may be greatly sub-divided as can be seen in the member of the family Sminthuridae illustrated in Figure 7A. They are usually equipped with sensory structures which can be very complex as can be seen in Figure 7B-D. Primitive Collembola have eight separate small eyes on each side of the head which have a characteristic distribution shown in Figure 8 but these are often reduced or absent. In front of this, in many groups of Collembola, there is an organ unknown function called the post antennal organ. This structure can be simple but is often very complex (Figure 9).
Collembola consume a wide variety of foods from vegetation to nematode worms although most favor fungi, spores and decaying vegetable material. This diet is associated in most Collembola with the presence of complex chewing surfaces or molar plates on the mandibles (which can handle resistant material such as plant tissues) and short complex maxillae seen in Figure 10A. However, Collembola display an enormous variety of different mouthparts ranging from simple piercing-sucking structures (seen in Figure 10B) to elaborate mouthparts (as seen in 10C). The simple piercing-sucking structures are probably associated with feeding on the juices of fungi or other liquid foods. Some of the complex mouthparts are associated with feeding on other tiny animals such as rotifers. However, we have no idea what most of the complex mouthparts are specialized for.
The digestive tracts of springtails are very simple straight tubes; however, some genera of the family Neanuridae have giant salivary gland chromosomes similar to those seen in Drosophila and some other flies. A few Collembola have simple tracheae, but most lack any internal respiratory structures. All have a simple tubular dorsal heart.
As might be suspected from their favored diets, most Collembola are reducers, and live in litter, decaying wood, or soil, or under dead bark, stones or litter on the soil surface, where they play an important role in breaking down dead plant materials and controlling the bacteria and fungi. Many eat green plants, and these are particularly important in tropical regions. A few, such as Proisotoma grandiceps (Figure 11) are carnivores although most of such species can also feed upon dead and decaying animal and/or plant materials. Collembola generally have short generation times, with some reproducing in as little as three weeks after hatching. This, combined with their abundance in many habitats, makes them favorite foods of many small animals ranging from mites to beetles. Some forms such as Dacetine ants, are specialized for feeding on them. In many ways you can think of Collembola as filling the same roles in the small, anthropod-dominated, animal world that mice fill in the larger vertebrate-dominated, animal world.
As with mice, many species of Collembola appear to be compete with each other. Recent studies have shown that different species interact in at least three different ways to affect each other's population growth: 1) by direct contact, 2) by producing materials onto the ground on which they live which affect other individuals, and 3) by producing chemicals which can be borne through the air which have some affect on other individuals. The most remarkable thing is that the interaction between the species may be very different in the three different types of interaction. For example let us consider the interaction between our old friend Folsomia candida and a member of the family Hypogastruridae, Xenylla grisea (Figure 12). The latter has no effect upon the population growth of the former as the result of direct contact or materials produced on the ground; however it has a positive effect when only airborne chemicals are involved. On the other hand F. candida has a strong negative effect on the population growth of X. grisea in direct contact or production of materials on the ground, but a strong positive effect when only airborne chemicals are involved. Other species have a negative interaction in all three types of situation. This remarkable complexity of interaction has not been examined yet in other animals, so we do not know if it is a peculiar feature of just the Collembola.
We are not certain when the chemicals causing these interactions are nor how the animals affect each other's reproductive rates. However, we do know that there are sometimes hostile interactions between Collembola when food is scarce. In such interactions, the Collembola use their antennae as clubs to beat each other over the heads as shown in Figure 13. In severe fights they run around in a tight circle, beating each other over their rear ends in a kind of dogfight. Remarkably these fights become less frequent and less severe in some species as the animals become more crowded.
Most springtails can only survive, or at least be active, in humidity conditions near the saturation point. Surface life in drier conditions requires physiological adaptations which are not well understood. Most of the species which can remain active in relatively dry conditions have scales or dense hairs which retard water loss. Eggs are generally less sensitive to desiccation than the animals themselves. Eggs and adults of some species shrivel up in dry conditions but can resume development or activity when re-hydrated by rain; such species can exist in sites which are only temporarily moist. Members of some genera such as Folsomides even build "nests" of fecal pellets in which this suspended animation, or anabiosis, occurs. If soil layers do not dry completely, surface species may survive by restricting their activity to night. Some species survive dry hot periods by ecomorphosis - metamorphosing into physiologically inactive form. Such forms usually have vestigial mouthparts, non-functional digestive systems, low metabolic rates and an appearance so strikingly different from the normal stage that some were originally placed in different genera from their normal forms. With the onset of normal conditions they molt again, recovering the normal form and function. One great mystery concerning this phenomenon is that in many species it appears only in the males.
In contrast to their sensitivity to dry conditions, many Collembola are quite resistant to cold. Some species, such as the European "glacier flea," Isotoma saltans, are active on snow or ice at temperatures well below freezing. This species, and probably others, feed on pine pollen plant, fragments and other debris trapped on the glacier surface. Similar species are known from North American and elsewhere, including a record species found over 21,000 feet on Mount Everest. Collembola are also abundant at high latitudes, and extend closer to the poles than most terrestrial organisms. Indeed the closer one gets to the poles, the more springtails dominate the soil systems. In some arctic regions the soil is largely made up of Collembola fecal pellets. One of the simplest ecosystems known can be found in some inland areas of Antarctica, where the only macroscopic organisms are one species of lichen and one species of springtail. Some species of Collembola can thrive in high temperatures. One Hawaiian species lives primarily in volcanic vents with constant temperatures mostly between 90 degrees and 130 degrees Fahrenheit.
Most Collembola do not change strikingly in form from the first molt after hatching through their adult state. The number of setae increase. Body ratios, patterns, and pigmentation change. And of course structures associated with sex do not appear until sexual maturity. They are unusual in that many species have no fixed number of molts. They can keep molting indefinitely. At first they continue to grow with each molt, and eventually they shrink at each molt. Females continue to increase the number of eggs laid during each period between molts after sexual maturity, for a couple of molts. But then the number of eggs decrease and eventually they stop reproducing entirely but continue to molt. The world record number of molts so far is 52. Another unusual feature in a few springtails is the fact that sexual differentiation of males is, except for the family Sminthuridae, generally weak and appears only shortly before maturity. However, in some species the differences between males and females continue to increase with each molt, as long as the animals live.
Most Collembola are bisexual, but the human meanings associated with that term are hardly appropriate. Males deposit sperm packets or spermatophores which are picked up by females which encounter them, and the sexes do not recognize each other. However, some members of the family Sminthuridae have elaborate courtship and spermatophore transfer techniques. For example, males of the genus Sminthurides, most of which live on water surfaces, have elaborate grasping antennae (Figure 14B) which they use to seize the female antennae. In some cases a pair may remain together for long periods of time with the female carrying the usually much smaller male suspended above the surface or every upside down on her back as is shown in Figure 14A. Periodically, in response to unknown cues, the male is lowered to the water surface. He deposits a spermatophore, and then guides the female to bring her genital opening into contact with it, whereupon the spermatophore ruptures and the female takes up the sperm. Another complex pattern is seen in the genus Bovicornia. Here the male has highly specialized structures on the forehead (Figure 15B) which he moves back and forth over the female's head (Figure 15A). This stimulates the female and the male turns around and secretes a sperm droplet (Figure 15C). The female picks it up with her mouth, deposits on the ground and then turns around and pushes it into her genital opening as shown in Figures 15D and E. Other members of the family have even more complex sexual activity. The members of this family are usually brightly colored and patterned; this is very probably associated with species and sex identification.
Another adaptation found in some Collembola is parthenogenesis where eggs do not need to be fertilized to develop and only females exist. This is found in Folsomia candida (shown in Figure 3). In this species most populations are parthenogenetic but some populations have both males and females. Other forms, particularly those found in caves or in deep soil layers where the chance of contact between the sexes is low, have species which are always parthenogenetic. For the deep soil forms of genus Tullbergia (Figure 16), almost all species are parthenogenetic.
This genus, which is one of many living primarily in the small spaces between soil particles, shows another characteristic of Collembola - the relationship between body form and habitat. This form belongs to a family primarily adapted to this habitat, the family Onychiuridae. All have lost eyes, furcula and pigment and have developed short antennae with elaborate antennal sensory structures (Figure 17A). Very elaborate post antennal organs as can be seen in the genus Onychiurus shown in the same figure. In spite of the lack of furcula, these forms are not without defense. The small openings or pseudopores shown by the arrow are scattered over the body and head. These structures are openings through which the animals can voluntarily release small quantities of their blood which is repellent, or in some cases even poisonous, to predators. It is amusing to watch an ant which has seized one of these animals drop it and try vigorously for a long while to wipe off its mouthparts. Short antennae, reduced or absent furcula, lack of eyes and pigment and complex sensory structures are characteristics of a wide array of genera which have independently evolved adaptations for this habitat.
In striking contrast to this set of characteristics, those species adapted to living above the ground, particularly those living on vegetation, tend to have bright colors, clear patterns, strongly developed furculas, and well-developed eyes and antennae. The members of the families Entomobryidae and Sminthuridae, seen in the bottom two illustrations on the cover, show this type of appearance. Many species are only found in the tree tops both in temperate areas and, more commonly, in the tropics. In species living in trees in tropical rain forests this body from reaches an extreme such as shown in Campylothorax (Figure 18). These forms have remarkable jumping abilities.
Many springtails living on water surfaces, such as Sminthurides aqauticus, are similar in some respects to the forms living in vegetation (Figure 14B) but have a furcula adapted to jumping on water. Look closely at the end of the furcula and you can see the end piece of mucro is broadened like a beaver's tail. They also have feet specially adapted for running over water surfaces. They are very common along the margins of lakes, ponds, streams and in marshes. They are an important food source for aquatic insects and young fish.
Caves are another habitat with conditions very favorable for Collembola. In spite of this, and the fact that many individuals accidentally fall or are swept into caves, relatively few species can survive and reproduce in caves. Almost all surfaces species such as Folsomia candida which are found in caves, are opportunistic invaders, unable to face competition from species which are specially evolved for cave life. The opportunistic forms are trapped by water pools and have difficulty moving over the water-filmed surfaces. The forms which have evolved for a long time in caves (called troglomorphs) have feet adapted for water surfaces and run over them with ease. Collembola make many evolutionary adaptations to caves, including conspicuous elongation of appendages and increased size. These evolutionary changes have occurred independently in cave systems all over the world to produce highly evolved members of different genera and tribes, all resembling the large Pseudosinella christianseni (Figure 19). Whether you are looking at caves in Australia, Europe, North America or Japan you can be certain that highly evolved cave forms of the family Entomobryidae will look like this. These forms bear a striking superficial similarity in body form to species found in the trees in tropical regions. However, unlike them they lack both pigment and eyes and their feet resemble those seen in aquatic species such as Sminthurides aquaticus. In lack of pigment or eyes, they resemble the deep soil forms.
Cave Collembola also show striking physiological adaptations for cave life. As springtails evolve species become more and more adapted to cave life, they tend to become intolerant of minor changes in environmental conditions, even though some species have lost the ability to detect and respond to such changes. In contrast to this delicacy in relation to physical conditions, many of these cave forms have a remarkable capacity to endure starvation, and some remain alive in culture for more than two years with only distilled water added to a bare substrate of charcoal and plaster.
Collembola may not actually be quite as indifferent to the food supply as this observation suggests. While they may prefer certain foods, most species are capable of surviving on a wide variety of materials, including fecal matter and bacteria. Thus they are able to reprocess their own wastes. In one experiment with specimens living on clay, it was found that the organic matter of the surface layer had increased after 8 months during which only distilled water had been added. According to an even more remarkable report, a population of Folsomia candida increased in numbers on a substrate of glass beads to which only distilled water was added. A possible explanation of this apparent violation of the laws of thermodynamics is that the Collembola were obtaining energy not only from their own cast skins and feces but from microorganisms introduced into the culture as airborne spores.
Sand dunes are another habitat where food would appear to be scarce for springtails. In addition their frequent extremely dry nature would make dunes appear to be very hostile environments for Collembola. Nevertheless recent studies have shown that if one moistens soil from sand dunes lightly for a number of days, large numbers of Collembola often emerge. This points out that the ability to survive complete drying by anabiosis is probably much more widespread than we had originally suspected. But the mystery of what they eat remains.
Another habitat which would appear to be hostile to Collembola is the inundated forest of the Amazon. This habitat where the forests are inundated for up to five months each year is just beginning to be studied. Not surprisingly there are many species of springtails which thrive in the trees; but very surprisingly it has been recently discovered that many Collembola, along with mites, are alive and active under the water on the forest floor when it is covered by water. It will be very interesting to discover what kinds of adaptations allow them to do this.
In contrast to these habitats, ant and termite nests are environments where we would expect Collembola to thrive. With high humidities and a variety of potential foods, the main problem is to escape the attention of the ants. The fact that relatively few groups of springtails are able to survive here indicates that this may be a serious problem. One family - Cyphoderidae - (see Figure 20) appears to ideally suited for this. Most species of the family are primarily or exclusively inhabitants of ant or termite nests. We know little of how they behave in the nest to escape being killed by their hosts but they are accepted. If you were to examine one of the columns of army ants which sweep across the floors of South American rain forests, you would find Collembola marching along with the ants. One of the most remarkable habits of termite-loving (or termitophilous) Collembola is that some members of the genus Colabatinus commonly sit on the head of soldier termites (Figure 21). Soldiers are unable to feed themselves and when the workers feed them, our Collembola steal a bit of the food. If the soldier is disturbed, the movement of the jaws is detected by the springtail's antennae and it uses the furcula to quickly jump off.
Collembola are a very ancient group and the very first fossil specimens are from the middle Devonian period about 380 million years ago. Some of these forms do not belong to any modern group of Collembola but are members of a now extinct genus. Since this genus is a highly specialized one, it implies that Collembola were around a very long time before the Devonian. Springtails are also very persistent through evolutionary time. The first really good fossils of Collembola are from Oligocene amber about 33 million years ago. These species all belong to genera still around. Most of the species we see today were probably here long before we arrived on the scene, and many will probably be here long after we have gone.
You may ask if the Collembola are all this wild and wonderful, why do most people know so little about them? The first and foremost answer is that they are so small. I have always noted that even when trained cave biologists go into caves they find Collembola only one of three times where I find them when I go into the same caves. I feel that it is certain that if Collembola were the size of cats there would be whole zoos devoted to them.
A second reason for general ignorance is the fact that they are so small that it takes special techniques to collect them. One easy way to collect is to make a simple aspirator such as shown in Figure 22. You will need a small jar filled with alcohol containing a number of small vials, a pair of small pincers, cotton and an aspirator. When you wish to make a collection you place a small vial, about 1/2 full of alcohol, in the large vial or tube as shown. To collect the specimen you point the intake at the springtail about 1 mm away and suck on the other tube sharply. The creatures stick in the alcohol in the small vial. After you have made all the collections you wish, remove the vial, put a label on it and use the pincers to plug it with cotton. Put this in the jar and take out another vial to start over. For examination under the compound microscope the animals can be mounted in Faure's medium or any other clearing mounting medium.
A third reason for people ignoring Collembola is that the good things they do for us are easy to ignore, and they really don't do much bad to us. The important role springtails have in recycling organic debris in the soil and probably even more important role in maintaining fungal and nematode concentrations favorable to plant growth is poorly studied. There are a few serious agricultural pests, most notable is the beautiful Lucerne Flea (Sminthurus viridis) in New Zealand and Australia which is a serious pest of alfalfa, but by-and-large Collembola are a harmless lot. There are no parasitic springtails of any sort, and the few examples of them infesting humans have been due to very peculiar circumstances. One of the most remarkable ones was a man who, collecting Collembola extensively in the Arctic with a leaky aspirator, manages to get a culture living in his nasal passages! He discovered this when Collembola started showing up on his handkerchief after he blew his nose. Other people who work around horses occasionally find Collembola living in their hair, but there have been few reports of this in recent years.
A fourth reason for general ignorance is that we have not found very many ways to use them so far. There have been some fairly successful attempts to use the Collembola fauna of the soil as indicators of the agricultural potential; this is used to some extent in Europe. Some springtails are extremely resistant to insecticides and some such as Folsomia candida can even digest DDT. It has been suggested that they might be used to decontaminate areas infested with these poisons but no extensive attempts have been made. Recent discoveries have shown that springtails are important in keeping root nematodes under control, and reducing infection by some soil borne pathogenic fungi. Again research into these areas is in very early stages. It is distinctly possible that we will make much greater use of them in the future.
In any case Collembola are really interesting animals and can be found everywhere. Next time you see little white creatures in a flower pot or tiny active blue-black specks on a patch of snow in a woods or on a tide pool, get a hand lens and look at them carefully. Better yet, start tearing off loose moist bark or turning over rocks and look for their scurrying bodies. Collect some and start identifying them. Soil Biology Guide published by Wiley and edited by Daniel Dindal, which should be available at any well equipped library, should enable you to do this.
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