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Sgardelis et al., 1981

Soil microarthropods are significant reservoirs ofbiodiversity but it is not clear exactly how diverse they may be. Estimation of species richness is a difficult problem for many types of soil organisms (fungi, bacteria and nematodes, for example, as well as microarthropods). In an extensive review, André et al. (2002) report that at most 10% of soil microarthropod populations have been explored and 10% of species described. Thus, according to those authors, the contribution of soil fauna to global biodiversity remains an enigma. Consequently, the mechanisms underlying the large species diversity of the microarthro-pods continue to elude us. The decline in numbers of taxonomic specialists for these groups has been noted (Behan-Pelletier and Bissett, 1993) as a contributing factor to our inadequate information base for microarthropods.

Unlike the macroarthropods, the mites and collembolans have little or no effect on soil structure. Their dimensions allow them to use existing spaces in soil structure. Even the large, soft-bodied members of the mite group Prostigmata do not seem to create their own passageways. Some litter-feeding species do burrow into substrates such as petioles of decaying leaves and create tunnels, but these have no direct effect on soil structure per se. The microarthropods resemble the microfauna in this characteristic.

Collembola

Among microarthropods, collembolans are often equal to soil mites in numerical abundance. They are worldwide in distribution and occur in all biomes, from tropic to arctic and from forest to grassland and desert and throughout the soil profile. Collembolans (Fig. 4.12) have the common name of "springtails" from the fact that many of the species are able to jump by means of a lever attached to the bottom of the abdomen. They also have a unique ventral tube (collophore), which seems to function in osmoregulation, and a springing apparatus (furcula and tenaculum) ventrally on the abdomen (absent in some groups). Most species are small, at most a few millimeters long, but may be brightly colored. They are ubiquitous members of the soil fauna, often reaching abundances of 100,000 or more per square meter. They occur throughout the upper soil profile, where their major diet appears to be fungi associated with decaying vegetation. In the rhizosphere, they are often the most numerous of the microarthropods. Surface-dwelling forms, inhabiting the litter layer, are usually well equipped with furculas (see Fig. 4.12). Residents of the deeper soil layers generally have no furcula, or only a rudimentary one, and typically lack pigmentation and eyes (Petersen, 2002).

The position of the Collembola in the world of arthropods continues to puzzle specialists. Classically these small, wingless arthropods have

FIGURE 4.12. (a) A symphypleonid collembolan (Sminthurus burtcheri) (Snider, 1969). (b) An arthropleonid collembolan (Isotomurus palustris) (Snider, 1967). (c) An onychiurid collembolan (Onychiuridae: Protaphorura sp.). Note the absence of the furcula (jumping apparatus) on the eyeless, soil-dwelling onychiurid, in contrast to the other litter-dwelling forms.

FIGURE 4.12. (a) A symphypleonid collembolan (Sminthurus burtcheri) (Snider, 1969). (b) An arthropleonid collembolan (Isotomurus palustris) (Snider, 1967). (c) An onychiurid collembolan (Onychiuridae: Protaphorura sp.). Note the absence of the furcula (jumping apparatus) on the eyeless, soil-dwelling onychiurid, in contrast to the other litter-dwelling forms.

been listed among the class Insecta (e.g., Boudreaux, 1979) but some authors suggest that they deserve a class of their own (Manton, 1970). Their mouthparts are held in a unique cone-shaped structure. Collem-bolans lack such features as compound eyes or wings, but do resemble insects by having three body regions. The head bears a pair of antennae. The thorax is three-segmented and bears three pairs of legs. The collembolan abdomen consists of only six segments, less than the insect model. The collembolan ventral tube, the collophore, is not found in other groups of arthropods.

The classification of the Collembola is relatively stable at the generic level, although many species remain unnamed and taxonomy of the group is based almost entirely on external morphology (Hopkin, 1997).

Resolution of the higher taxonomic categories will require a close examination of the fauna of the entire world (Christiansen and Bellinger, 1998). In North America, the taxonomic analysis by Christiansen and Bellinger (1998) is the standard reference and provides keys to genera and known species. On a worldwide basis, the literature is scattered over a wide variety of journals and other publications. Hopkin (1997) offers regional checklists of the collembolan fauna. The publications of Gisin (1962, 1963, 1964, and others cited therein) are essential for the study of European Collembola.

With the development of computerized access to the World Wide Web, another large array of resources has recently become available. A good search engine will locate several thousand Web sites referencing collembolans and offering keys, check lists, lists of specialists, and other valuable information. These resources include such assets as a world list of collembola, interactive keys to species in some of the genera, a list of references to Collembola beginning in 1995, and a catalog of the neotropical species. We anticipate that the World Wide Web will become even more valuable as a source of information about microarthropods. (We do not offer specific Web addresses because they are often subject to change.) A cautionary note: Web pages are seldom peer reviewed.

Identification of collembolans requires use of a microscope and magnifications as high as 400x. Preliminary sorting of samples to family levels can be performed with a dissecting microscope, once some familiarity with the group has been gained. Recognition of genera and species will require slide mounts (see Chapter 9). Collembolans will float on the surface of many collection fluids, due to their very hydrophobic cuticle, and special collection fluids are recommended (see Chapter 9).

Families of Collembola

In the current system of classification, a dozen or so families of collembolans are arranged in three major groups (Christiansen and Bellinger, 1998). The suborder Arthropleona contains the so-called "linear" collembola, the great majority of species, in two sections: the Poduromorpha and the Entomobryomorpha.

Poduromorph collembolans [Fig. 4.12(c)] include the important families Hypogastruridae and Onychiuridae, whose species are dwellers in mineral soil layers, and the family Poduridae with a single darkly pigmented species, Podura aquatica, whose natural habitat is standing water.

Onychiurid collembolans [Fig. 4.12(c)] almost always have no furcu-la; eyes are reduced or absent and, if present, are unpigmented. They possess pseudocelli, cuticular organs which have nothing to do with vision but which can extrude a defensive oil when disturbed, an alarm pheromone (Usher and Balogun, 1966). Onychiurids feed in the rhizos-phere. Curl and Truelove (1986) argue persuasively that these collem-bolans are attracted to plant roots and are important in rhizosphere dynamics. In experiments, collembolans protected cotton plants from the root pathogen Rhizoctonia solani by selectively grazing that fungus from the plant roots. These rhizosphere inhabitants may prove to be effective biological control agents (Fig. 4.13, Curl and Truelove, 1986). Onychiurids are not well sampled with Tullgren funnels; they do not appear to respond to the heating and drying process in Tullgren extractions. Estimates of numbers of Onychiurids are best made with flotation methods (see Chapter 9) (Edwards, 1991).

The family Hypogastruridae includes several common species whose populations may build up to huge numbers. These include the "snow flea," Hypogastrura nivicola. That species multiplies under winter snows and, on warm days, appears to boil out onto the surface (Christiansen, 1992). Another related species, H. armata, is common in the litter layer of hardwood forests during the winter months (Snider, 1967). We have found H. armata (Fig. 4.14) to be the predominant winter microarthropod in hardwood litterbags in the southern Appalachians (Crossley and Coleman, unpublished data).

The Entomobryomorpha [Fig. 4.12(b)] includes the large family Ento-mobryidae in which the furcula is well developed. The collembolans are primarily dwellers of surficial soil layers, in forest canopies or on tree trunks. Laboratory cultures of one species, Sinella curviseta, have found a valuable role as prey for cultures of spiders (Draney, 1997). Species in the family Tomoceridae (Fig. 4.15) include large forms with long antennae, found in upper litter layers of forest floors throughout the Holarctic region.

Members of the family Isotomidae are a highly variable set of species; the group is in need of serious taxonomic revision (Christiansen and Bellinger, 1998). This family includes Folsomia Candida (Fig. 4.16), a species widely used in laboratory experiments and in the assessment of the effects of toxic substances. Its reproductive biology has been thoroughly explored and culture methods well developed (Snider, 1973). In fact, the microbial gut flora of F. candida has been extensively explored using DNA probing methods. It was found to be a frequently changeable but selective habitat, possibly indicating that soil microarthropods could modify the species makeup of soil microbial communities (Thimm et al., 1998). The European "glacier flea," Isotoma saltans, is active on ice at temperatures below freezing and feeds on pollen grains trapped on the glacier surface (Christiansen, 1992).

The third major group of Collembola, the suborder Symphypleona, includes the spherical or globular collembolans. It is a smaller group than the Arthropleona and much more uniform in habits (Christiansen

FIGURE 4.13. Collembolan protection of roots from infection by Rhizoctonia solani. (Left) Roots from pathogen-infested soil with mycophagous collembola; (right) diseased root from pathogen-infested soil without collembola (from Curl and Truelove, 1986).
FIGURE 4.14. Drawing of Hypogastrura armata, common in wintertime in Coweeta forest floors, in western North Carolina in the United States (from K. Christiansen, with permission).
FIGURE 4.15. Tomocerus dubius (from K. Christiansen, with permission).
FIGURE 4.16. Folsomia candida adults and juveniles. The largest individual is 2mm in length (from Hopkin, 1997).

and Bellinger, 1998). The family Sminthuridae [Fig. 4.12(a)] is a large and cosmopolitan one, being active jumpers, dwellers in surficial litter layers, on vegetation, and in the canopies of tropical humid forests. Often brightly colored, these collembolans are readily collected with Tullgren funnels or pitfall traps (see Chapter 9), but may also be collected by sweeping through grassy vegetation with a white enamel pan. The family Neelidae consists of tiny globular forms lacking eyes and with short antennae. The family is cosmopolitan but poorly studied (Hopkin 1997).

Population Growth and Reproduction

Many collembolans are opportunistic species, capable of rapid population growth under suitable conditions. They often respond to disturbances of the soil environment. In agricultural systems, spurts of growth may follow plowing or cultivation (Hopkin, 1997). In forests, fire may stimulate collembolan abundances, as may the broadscale application of pesticides (Butcher et al., 1971). Collembolans occur in aggregations. In samples of soils, they are not found at random, but occur in groups. Aside from the statistical problems of assessment of population size, aggregations pose ecological questions as well. In laboratory investigations, Christiansen (1970) and Barra and Christiansen (1975) analyzed collembolan responses to habitat variables (i.e., moisture and substrate) and food resources. Although these were important, the major variable seemed to be a behavioral one. Collembolans possess aggregation pheromones (Krool and Bauer, 1987), which probably function in bringing the sexes together for reproductive purposes. Earlier, reproductive pheromones were identified by Waldorf (1974). Many collembolan species are capable of rapid, even explosive, population growth under ideal conditions. Gist et al. (1974) analyzed life tables for Sinella curviseta under laboratory conditions for 170 days; they found an intrinsic rate of increase of 0.036 per day and a replacement rate (Ro) of 515 per female.

Sperm transfer is by means of spermatophores, either actively passed or deposited on pedicels and located by the females. Eggs are laid in groups. Development is continuous; the number of instars ranges between 2 and 50 or more (Christiansen and Bellinger, 1998). Collem-bolans become sexually active with the fifth or sixth instar but continue to molt throughout life, in contrast with the Insecta, which do not molt after reproduction.

Parthenogenic reproduction is common in many collembolan species, including the commonly cultured Folsomia candida. Many species are bisexual, especially those in the Entomobryidae (e.g., Sinella curviseta).

Collembolan Feeding Habits

Collembolans are generally considered to be fungivores, with occasional ingestion of other animals, decomposing plant or animal residue, or fecal material. As noted previously, they are often considered to be nonspecific feeders but this conclusion is controversial (Petersen, 2002). Gut content analysis of field-collected specimens or field observation in rhizotrons (Gunn and Cherrett, 1993) often reveals a wide variety of materials, including fungi, plant debris, and animal remains. Laboratory choice studies, in contrast, have found that collembolans have specific food preferences, choosing one fungal species over others (similar discrepancies in feeding analysis have been noted for oribatid mites; see later section on mites). Bengtsson et al. (1994), in laboratory experiments, reported that the collembolan Protaphorura armata showed an increased dispersal rate if a favored fungus was present as far away as 40 cm (cited in Petersen, 2002).

Models of soil food webs usually place collembolans as fungivores (e.g., Coleman, 1985; Hunt et al., 1987; Moore and de Ruiter, 2000). However, like many of the soil fauna, collembolans in general defy such exact placement into trophic groups. Living plant tissue may be consumed and even dead animal material or feces in cultures. Many collembolan species will eat nematodes when those are abundant (Gilmore and Potter, 1993). Some species may be significant in the biological control of nematode populations (Gilmore, 1972). Feeding on nematodes does not seem to be selective; collembolans do not distinguish between saprophytic and plant parasitic nematodes. In the words of Hopkin (1997), "Indeed the opportunistic nature of the feeding behaviour of many species of Collembola may be one reason for their success."

Collembolan Impacts on Soil Ecosystems

The direct effect of collembolans on ecosystem processes such as energy flow appears to be quite small. Their biomass is relatively tiny, their respiration rates are but a small fraction of total soil CO2 efflux, and their feeding rates account for only a small amount of microbial activity. They share these characteristics with other soil microarthropods (Gjelstrup and Petersen, 1987). These conclusions have lead Andren et al. (1999) to a sardonic statement, to wit: "Soil animals exist. I like soil animals. They respire too little. Ergo, they must CONTROL something!" Those authors caution us to avoid an overly enthusiastic appraisal of the importance of microarthropods in soil ecosystems. Nevertheless, manipulation experiments have shown important impacts of collembola on nitrogen mineralization, soil respiration, leaching of dissolved organic carbon, and plant growth (Filser, 2002). These system responses may be viewed as indirect effects. Assessing the importance of Collembola in soil ecosystems needs to be done in the context of the intact system and may be expected to vary with temperature, moisture, season, and interactions with other biota.

Grazing upon fungal hyphae appears to be the major contribution of Collembola in the decomposition process. Such grazing on fungal hyphae may be selective, thus influencing the fungal community (Table 4.3). Indirectly, such direct effects on the fungal community may have indirect effects on nutrient cycling (Moore et al., 1987). Selective grazing by the collembolan Onychiurus latus changed the outcome of competition between two basidiomycete decomposer fungi (Newell, 1984a, b), allowing an inferior competitor to prosper. Grazing upon fungi may actually increase general fungal activity in soils and stimulate fungal growth. The relationship between fungal and collembolan population dynamics is not straightforward, however, because some collembolan species may actually reproduce more successfully on least favored foods (Walsh and Bolger, 1990). Collembola have been demonstrated to have complex interactions with several fungal species simultaneously. Cotton was grown in a greenhouse with four fungal species, the pathogen Rhizoctonia solani and three known biocontrol fungi (including two sporulating Hyphomycetes), and the rhizosphere-inhabiting collem-bolan Proisotoma minuta. The collembolan preferentially fed on the pathogenic fungus and avoided the biocontrol fungi (Lartey et al., 1994).

Acari (Mites)

The soil mites, Acari, chelicerate arthropods related to the spiders, are the most abundant microarthropods in many types of soils. In rich forest soil, a 100-g sample extracted on a Tullgren funnel may contain as many as 500 mites representing almost 100 genera (Table 4.4). This much diversity includes participants in three or more trophic levels and varied strategies for feeding, reproduction, and dispersal. Often, ecolo-gists analyze samples by a preliminary sorting of mites into suborders. Identification of mites to the family level is a skill readily learned under

TABLE 4.3. Compensatory Growth of Fungi in Response to Collembolan Grazing

Fungal species

Collembolan species

Growth relative to controls

Botrytis cinerea

Folsomia fimetaria

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