Springtail

Foraging

Specific feeding (foraging) strategies and mechanisms are employed to match specific niches.^[52] Herbivorous and detritivorous species fragment biological material present in soil and leaf litter, supporting decomposition and increasing the availability of nutrients for plants and various species of microbes and fungi.^[53][54] Carnivorous species maintain populations of small invertebrates such as nematodes, rotifers, and other collembolan species.^[4][25] Springtails commonly consume fungal hyphae and spores, but also have been found to consume plant material and pollen, animal remains, colloidal materials, minerals and bacteria.^[55] Streptomyces actinobacteria produce geosmin which attracts some species of springtails which feed on and spread their spores.^[56] Some springtail species like Anurophorus laricis can form mutually beneficial relationships with lichens, using them for shelter while feeding on surrounding free-living algae, which helps reduce competition between algae and lichens for space and nutrients.^[57] For finding their preferred food in light-free and complex environments like litter and soil layers Collembola use olfactory cues such as the odors emitted by fungi and other food sources as attractors.^[58] Directional movement towards the food source has been recorded by image analysis in laboratory experiments.^[59] However, other experiments showed that attraction and consumption were often, but not always correlated, and that preferred fungal strains were not necessarily those that optimize performances in reproduction (fitness), growth and survival.^[60]

Predators

Springtails are consumed by mesostigmatan mites in various families, including Ascidae, Laelapidae, Parasitidae, Rhodacaridae and Veigaiidae.^[61] Cave-dwelling springtails are a food source for spiders and harvestmen in the same environment, such as the endangered harvestman Texella reyesi.^[62] Predators also include various soil centipedes.^[63]

Jumping, using the furcula as a spring, is the most common way to avoid predation,^[64] but jump escape cannot be performed easily in concealed environments such as litter, and more especially soil layers. To protect themselves against predators, some species without jumping abilities have evolved chemical defenses.^[65]

Distribution

Springtails are cryptozoa frequently found in leaf litter and other decaying material,^[4] where they are primarily detritivores and microbivores, and one of the main biological agents responsible for the control and the dissemination of soil microorganisms.^[66] In a mature deciduous woodland in temperate climate, leaf litter and vegetation typically support 30 to 40 species of springtails, and in the tropics the number may be over 100.^[4]

In sheer numbers, they are reputed to be one of the most abundant of all macroscopic animals, with estimates of 100,000 individuals per square meter of ground,^[67] essentially everywhere on Earth where soil and related habitats (e.g. moss cushions, fallen wood, grass tufts, ant and termite nests) occur.^[68] Only nematodes, crustaceans, and mites are likely to have global populations of similar magnitude, and each of those groups except mites is more inclusive. Though taxonomic rank cannot be used for absolute comparisons, it is notable that nematodes are a phylum and crustaceans a subphylum. Most springtails are small and difficult to see by casual observation, but some springtails, like snow fleas, are readily observed on warm winter days when it is active and its dark color contrasts sharply with a background of snow.^[69][70]

In addition, a few species routinely climb trees and form a dominant component of canopy fauna, where they may be collected by beating or insecticide fogging.^[71][72] In temperate regions, a few species (e.g. Anurophorus laricis, Entomobrya albocincta, Xenylla xavieri, Hypogastrura arborea) are almost exclusively arboreal.^[68] In tropical regions a single square meter of canopy habitat can support many species of Collembola.^[73]

The main ecological factor driving the local distribution of species is the vertical stratification of the ecosystem: in woodland a continuous change in species assemblages can be observed from tree canopies to ground vegetation then to plant litter down to deeper soil horizons.^[68] This is a complex factor embracing both nutritional and physiological requirements, together with behavioural trends,^[74] dispersal limitation^[75] and probable species interactions.^[76] Some species have been shown to exhibit negative^[77] or positive^[74] gravitropism, which adds a behavioural dimension to this still poorly understood vertical segregation. Experiments with peat samples turned upside down showed two types of responses to disturbance of this vertical gradient, called stayers and movers.^[78]

As a group, springtails are highly sensitive to desiccation, because of their tegumentary respiration,^[79] although some species with thin, permeable cuticles have been shown to resist severe drought by regulating the osmotic pressure of their body fluid.^[80] The gregarious behaviour of Collembola, mostly driven by the attractive power of pheromones excreted by adults,^[81] gives more chance to every juvenile or adult individual to find suitable, better protected places, where desiccation could be avoided and reproduction and survival rates (thereby fitness) could be kept at an optimum.^[82] Sensitivity to drought varies from species to species^[83] and increases during ecdysis.^[84] Given that springtails moult repeatedly during their entire life (an ancestral character in Hexapoda) they spend much time in concealed micro-sites where they can find protection against desiccation and predation during ecdysis, an advantage reinforced by synchronized moulting.^[85] The high humidity of many caves also favours springtails and there are numerous cave adapted species,^[86][87] including one, Plutomurus ortobalaganensis living 1,980 metres (6,500 ft) down the Krubera Cave.^[88]

The horizontal distribution of springtail species is affected by environmental factors which act at the landscape scale, such as soil acidity, moisture and light.^[68] Requirements for pH can be reconstructed experimentally.^[89] Altitudinal changes in species distribution can be at least partly explained by increased acidity at higher elevation.^[90] Moisture requirements, among other ecological and behavioural factors, explain why some species cannot live aboveground,^[91] or retreat in the soil during dry seasons,^[92] but also why some epigeal springtails are always found in the vicinity of ponds and lakes, such as the hygrophilous Isotomurus palustris.^[93] Adaptive features, such as the presence of a fan-like wettable mucro, allow some species to move at the surface of water in freshwater and marine environments.^[94] Podura aquatica, a unique representative of the family Poduridae (and one of the first springtails to have been described by Carl Linnaeus), spends its entire life at the surface of water, its wettable eggs dropping in water until the non-wettable first instar hatches then surfaces.^[95] A few genera are capable of being submerged, and after molting young springtails lose their water repellent properties and are able to survive submerged under water.^[96]

In a variegated landscape, made of a patchwork of closed (woodland) and open (meadows, cereal crops) environments, most soil-dwelling species are not specialized and can be found everywhere, but most epigeal and litter-dwelling species are attracted to a particular environment, either forested or not.^[68][97] As a consequence of dispersal limitation, landuse change, when too rapid, may cause the local disappearance of slow-moving, specialist species,^[98] a phenomenon the measure of which has been called colonisation credit.^[99][100]

Role in turfgrass ecosystems

In managed turfgrass and urban lawn ecosystems, Collembola function as "thatch busters", playing a significant role in the decomposition of thatch, i.e. the layer of living and dead organic matter between the green vegetation and the soil surface. A common model species in North American turfgrass is Isotomiella minor.^[101]

Relationship with humans

Springtails are well known as pests of some agricultural crops. Sminthurus viridis, the lucerne flea, has been shown to cause severe damage to agricultural crops,^[102] and is considered as a pest in Australia.^[103][104] Onychiuridae are also known to feed on tubers and to damage them to some extent.^[105] However, by their capacity to carry spores of mycorrhizal fungi and mycorrhiza helper bacteria on their tegument, soil springtails play a positive role in the establishment of plant-fungal symbioses and thus are beneficial to agriculture.^[106] They also contribute to controlling plant fungal diseases through their active consumption of mycelia and spores of damping-off and pathogenic fungi.^[107][108] It has been suggested that they could be reared to be used for the control of pathogenic fungi in greenhouses and other indoor cultures.^[109][110]

Springtails sometimes find their way inside human living spaces. However, most pesticides are not effective against them and moisture-removal strategies are the best line of defense to combat infestations.^[111]

Various sources and publications have suggested that some springtails may parasitize humans, but this is entirely inconsistent with their biology, and no such phenomenon has ever been scientifically confirmed, though it has been documented that the scales or hairs from springtails can cause irritation when rubbed onto the skin.^[112] They may sometimes be abundant indoors in damp places such as bathrooms and basements, and incidentally found on clothes or skin.^[111] More often, claims of persistent human skin infection by springtails may indicate a neurological problem, such as delusional parasitosis or pareidolia, a psychological rather than entomological problem.^[113] Researchers themselves may be subject to psychological phenomena. For example, a publication in 2004 claiming that springtails had been found in skin samples was later determined to be a case of pareidolia; that is, no springtail specimens were actually recovered, but the researchers had digitally enhanced photos of sample debris to create images resembling small arthropod heads, which then were claimed to be springtail remnants.^{[112][114][115][116][117]} However, Steve Hopkin reports one instance of an entomologist aspirating an Isotoma species and in the process accidentally inhaling some of their eggs, which hatched in his nasal cavity and made him quite ill until they were flushed out.^[4]

In 1952, during the Korean War, China accused the United States military of spreading bacteria-laden insects and other objects during the Korean War by dropping them from P-51 fighters above rebel villages over North Korea, an allegation of bacterial warfare. In all, the U.S. was accused of dropping ants, beetles, crickets, fleas, flies, grasshoppers, lice, springtails, and stoneflies as part of a biological warfare effort. The alleged associated diseases included anthrax, cholera, dysentery, fowl septicemia, paratyphoid, plague, scrub typhus, small pox, and typhoid. China created an international scientific commission for investigating possible bacterial warfare, eventually ruling that the United States probably did engage in limited biological warfare in Korea. The US government denied all the allegations, and instead proposed that the United Nations send a formal inquiry committee to China and Korea, but China and Korea refused to cooperate. U.S. and Canadian entomologists further claimed that the accusations were ridiculous and argued that anomalous appearances of insects could be explained through natural phenomena, but speculation to this day exists as to whether the U.S. may have been experimenting in the field during the Korean war.^[118] Springtail species cited in allegations of biological warfare in the Korean War were Isotoma (Desoria) negishina (a local species) and the "white rat springtail" Folsomia candida.^[119]

Captive springtails are often kept in a terrarium as part of a clean-up crew.^[120]

Ecotoxicology laboratory animals

Springtails are currently used in laboratory tests for the early detection of soil pollution. Acute and chronic toxicity tests have been performed by researchers, mostly using the parthenogenetic isotomid Folsomia candida.^[121] These tests have been standardized.^[122] A ringtest on the biology and ecotoxicology of Folsomia candida, compared with the sexual nearby species Folsomia fimetaria (sometimes preferred to Folsomia candida), was performed by 14 participating laboratories and concluded that both species could be proposed for acute and chronic toxicity testing.^[123] At first sight care should be taken that different strains of the same species may be conducive to different results. A study comparing two RAPD-defined clones of Folsomia candida did not reveal significant sensitivity differences throughout a concentration gradient of cadmium,^[124] while another study comparing two strains of the same species and the same contaminant (cadmium) came to the reverse conclusion.^[125]

Avoidance tests have been also performed,^[126] also showing that different strains of Folsomia candida responded differently. Avoidance tests have been standardized, too.^[127] Avoidance tests are complementary to toxicity tests, but they also offer several advantages: they are more rapid (thus cheaper), more sensitive and they are environmentally more reliable, because in the field Collembola move actively far from pollution spots.^[128] It may be hypothesized that the soil could become locally depauperated in animals (and thus improper to normal use) while below thresholds of toxicity.^[129]

Contrary to earthworms,^[130] but see^[131] and like many insects^[132] and molluscs,^[131] Collembola are very sensitive to herbicides.^[133][134]

The springtail Folsomia candida is also becoming a genomic model organism for soil toxicology.^[135][136] With microarray technology the expression of thousands of genes can be measured in parallel. The gene expression profiles of Folsomia candida exposed to environmental toxicants allow fast and sensitive detection of pollution, and additionally clarifies molecular mechanisms causing toxicity.^[137]

Collembola have been found to be useful as bio-indicators of soil quality.^[138] Laboratory studies have been conducted that validated that the jumping ability of springtails can be used to evaluate the soil quality of Cu- and Ni-polluted sites.^[139]