Springtails 400-360mya

Mycorrhiza Plants Animals Arachnids Worms Greening

Springtails

In healthy soil, we can find upwards of 100,000 of these creatures in a square metre. Somebody has calculated that soil springtail biomass worldwide at 27.5 megatons carbon, which is 3X wild terrestrial vertebrates“. (Potapov 2023) They must be playing a massive role in soil

According to USDA entomologist Ian Stocks, Collembola can be thought of as “cows of the forest floor” since by their great abundance they are a major food source for the many small predators that roam the same environments,

Many predators of springtails – like mites, centipedes and spiders - have evolved over the years, although beetles were latecomers around 60mya.

After springtails sprung along water films following the 'earth smell' and finding sanctuary in moss, did they now go out and find food round newly formed roots?

Survival

Collembola have a gregarious behaviour mostly driven by the attractive power of pheromones excreted by adults. This 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. Springtails also possess the ability to reduce their body size by as much as 30% through subsequent moulting, if temperatures rise high enough. The shrinkage is genetically controlled. Since warmer conditions increase metabolic rates and energy requirements in organisms, the reduction in body size is advantageous to their survival. Two springtail families - Isotomids and Hypogastrurids - which live in litter layers, can go through a period of reduced activity. They develop a unique morphology, with heavy abdominal spines and wrinkled surface, as well as reduced mouthparts and digestive systems as they also stop feeding. This – ecomorphosis - comes most commonly with drying or high temperature. When decent conditions return, there is a quick moult and they return to normal anatomy and activity. Other springtails avoid heat by climbing plants during the day and returning to earth at night.

Springtails respire through a porous cuticle, not a tracheal system like insects, with the notable exception of the Sminthuridae, which exhibit a rudimentary, although fully functional, tracheal system.

Springtail skin, or cuticle is an omniphobic material, capable of repelling dirt, water, even oil. They are very clean creatures, rarely seen with debris[CH18] , oil or water on them. This skin is being studied as a meta material for industry applications. Springtail cuticle has many advantages as its build is unlike anything else in nature, and comes from a probable evolutionary adaption to maintain skin respiration in flooded and over-damp soil environments.“They have evolved a non-adhesive surface that exhibits a unique hierarchical structure consisting of micro-scaled bristles and granules (tertiary and secondary structure) and a comb-like alignment of smaller mushroom-shaped granules with interconnecting ridges (primary structure)(Hannig et al 2018). They have a strong wetting resistance, throwing off water, that makes their structure interesting for anti-fouling applications.

Getting back to the roots

We saw that around 1/2 bya springtails sprang along water films following the geosmin smell, indicating bacteria ahead. Spreading out from standing water would offer new environments for them and explain their strange structures. We saw how they can surf the films and spring great distances, perhaps landing in mosses where they have been living for millions of years. But now new opportunities with the growth of roots were opening up. Springtails, being generalist feeders found something else to eat - fungi,

Plants pass the energy captured from the sun by photosynthesis, as sugars to the fungi in their new emerging roots. These sugars, as well as glomalin, thus transfers carbon from plant to fungi to springtails to the soil. and ultimately the soil, making the soil a 'carbon sink'.

They enhance the flow of organic carbon by fragmentation and restructuring of organic matter and with densities in the range of 104 specimens per m2 are being examined more closely as we look more at carbon in soil.

The amount of organic carbon stored in soils is about three times that in living plants and double that in the atmosphere. This is a relatively new term, and may give the impression the carbon is trapped, whereas it is really in a state of flux. The springtails play a vital role in moving the carbon around.

Springtails, nowadays, are crucial to many soil ecosystems. Some eat bacteria, others fungi, and others digest debris, but all - 27.5 megatons of them - provide food for others. But which ones were around all those years ago, and what were they doing?

Digestion

Springtails are primarily fungivores, but also food generalists and may feed on a great variety of resources, bacteria, mosses, spores, decaying plants, and organic debris.

They use their scraping mouthparts to feed on fungal hyphae and microorganisms on the surface of organic matter.

They pay more attention to the moisture levels, rather than anything else, meaning they do not rely on any particular fungus, but rely on being around in moist conditions.

Tomocerid mouthparts to shear the food particles or grind the fragments. Illustration adapted from Biology of the Sprintails. S.P. Hopkin, from Atlas of the Biology of Soil Arthropods - G.Eisenbeis and W.Richard (1985)

A large proportion of springtails primarily feed on fungi, including mycorrhizal fungi and fungi growing on decaying organic matter. They help control fungal populations and play a significant role in fungal dynamics in the soil. They are secondary feeders on detritus: While their main diet is fungi, springtails may also consume decomposing organic matter, especially when fungi are growing on it. However, they do not typically chew large pieces of detritus but rather scrape off the fungal hyphae and other microorganisms from the surfaces.

Gut

Compared with those of other soil invertebrates, gut sizes of these microarthropods are several orders of magnitude smaller. They have well-developed mouth parts to cut up organic substances, increasing the surface areas of the substrates to make them more accessible for microbial action. Passing through the gut enhances rates of decomposition by inoculating the organic material with bacteria, which are predominantly aerobic, enabling them to continue to grow in the faeces (Thimm et al., 1998)

Springtails have a well developed digestive system consisting of an intestine divided into three distinct parts. Most families have chewing mouthparts. This section of an Arthropleone springtail, the sort that were around 350mya, starts with a mouth, having salivary glands whose function is to secrete enzymes that will be mixed with food in the oral cavity. After the pharynx, the anterior intestine is prolonged by a gullet that delivers food to the midgut, a large pocket surrounded by a network of muscles. The contractions of this muscular network make it possible to knead the food and to evacuate it to the posterior intestine. The interior of the midgut is lined with digestive cells that secrete enzymes capable of absorbing the products of digestion.

Enzymes

Microorganisms provide the metabolic basis for nutrient cycling in soil. In undisturbed soils, these microorganisms are often in plant rhizospheres or guts of soil animals. These ecological niches have higher concentrations of nutrients and increased microbial biomass (Thimm et al., 1998). In open soil, most bacterial cells are more or less in the status of starvation. Life is much better in the guts of small soil animals.

The level of acidity (pH starts around 8 - blue- then around 6, mildly acidic) in the intestinal pocket is maintained at an optimal value to allow these enzymes to fulfill their role. Some species of springtails such as Pogonognathellus flavescens secrete cellulase which is an enzyme capable of digesting cellulose. A “majority of the samples analysed showed trehalase and cellulase activity, and indicate that Collembola commonly have the ability to digest cell walls of plants and algae, and the contents of fungal hyphae. Most of the species examined had chitinase activity, and are able to digest fungal cell walls”(Berg, Stoffer, and van den Heuvel, 2004) If anything can digest the difficult glomalin it would be these enzymes.

This digestion allows them to play an essential role in the transformation of organic matter through their droppings which take place under form small faecal pellets. The latter take shape in the rectum after the water contained at the exit of the midgut has been absorbed by the cells of the posterior intestine.

IN - AMF

Different Collembola species have a preference for different AMF species. They are not 'fussy' fungal feeders'.

Scanning electron microscopy (SEM) detected the presence of fungal mycelia and some bacterial cells in the gut of the soil collembolan Folsomia candida. It was concluded that the presence of fungi was primarily a result of the ingestion of fungal hyphae as a food substrate (Thimm et al 1998)

Most investigations of collembolan guts find traces of fungal matter but v few intact spores.

Fungal exudate glomalin

Bardgett, Whittaker & Frankland, 1993a, 1993b; Tiunov & Scheu, 2005.

OUT - Aggregates

Poo out GRSPs,

Rillig 2004 "GRSP concentrations in soil are positively correlated with aggregate water stability. GRSP has relatively slow turnover in soil, contributing to lasting effects on aggregation. "

Few studies have examined collembola effects on soil aggregation. A greenhouse study asked about the effect of collembola on soil aggregation and whether it altered AM fungi-mediated effects. Using two different plant species, the study showed that both AM and collembola improved aggregates, and “moreover, the interaction effects between AMF and collembola were significant…Our findings show that collembola can play a crucial role in maintaining ecological sustainability through promoting soil aggregation, and point to the importance of considering organism interactions in understanding formation of soil structure.”(Siddiky et al., 2012) This supports my theory that springtails can break down glomalin and turn into GRSPs that stick soil together

Fungi

While they may have started off eating bacteria and nematodes, perhaps also microalgae, they have become primarily fungivores (ie eat fungi), both mycorrhizal and saprophytic. They may well also be detrivores, as they do not appear to be too picky.

“Labelled C was primarily found in fungal fatty acid biomarkers (and rarely in bacterial biomarkers), and in Collembola, but not in Acari and Enchytraeidae” worms."(Hogberg et al., 2010) They showed the amount of such carbon was much greater later in the season.

I would like to postulate that lots of small soil animals, particularly springtails, eat a lot of the glomalin from the fungi as they nibble round the roots . This plays an important role in two functions – spore dispersal and aggregate formation. They eat significant amounts of glomalin, digesting it with the actions of gut bacteria, and defecating the result, while accidently passing on spores. Both these actions have major impacts on soil formation. They do a lot of chewin’, pooin’ and gluein’ to create soil life. The science isn’t here yet to ‘prove’ this, but there are a lot of pointers as to how these creatures link many soil processes together..

I remember looking at springtails on apple tree roots, over 50 years ago, in the ‘Root Laboratories’ at East Malling Fruit Research station. It is famous for its ‘Malling’ rootstocks sold all over the world. It’s a shame the Research station doesn’t benefit from that now. The root labs built there were to measure the length and sizes of various rootstocks so as to better calculate how big a tree would grow to fit your plot. However, I was more interested in loads of little white creatures sniffling about and nibbling the roots. These springtails were I think called Onychiurids. I wondered what they were doing and why I’d never heard about them. It is that which stimulated my interest in soil life. It is has taken over 50 years to work out what they may be doing; eating bits of roots and fungi. And in so doing passing on spores, energy and minerals to others. Here was some chewin’, pooin’, and gluein’.

Abundant and diverse fungal matter and bacterial propagules are found in the guts of Collembola. Some fungal spores are eaten and can pass through the springtail guts. One set of results suggest that dispersal of intact spores of two fungi, Inocybeand Mycena after ingestion by Morulina is possible (Nakano et al., 2017). However elsewhere studies with deeper living Onychurids, only 50% of the pellets contained viable propagules. “While bacteria spores go through, A significant reduction in spore viability as a result of gut passage through Collembola has been demonstrated for a range of fungi. Damage to fungal hyphae and spores during gut passage may explain the greater number of fungal propagules and taxa associated with the exterior of each 0. subtenuis (2.5 -5.1 propagules, 1.8-3.7 taxa) than the number associated with each viable faecal pellet (1-1.3 propagules, 0.8- 1.3 taxa).

Microalgae

Soil microalgae can be very productive and contribute to the diet of many soil decomposers such as Collembola. Using 15N/14N ratios we showed that phycophagy is of particular importance for Collembola in extreme habitats like rock surfaces, or seasonally during the wintertime. In such situations, non-vascular plants can represent the major part of the diet of Collembola". (Potapov 2018). These may well have been the sorts of conditions they would have faced 400mya.

Folsomia

Bacteria in their guts

The midgut may contain other symbiotic living bacteria capable of making certain enzymes that springtail does not produce naturally. Springtails eat bacteria. As we’ve seen they can detect bacterial spores which some bacteria release, with accuracy because of the smell of geosmin. Interaction between springtails and microorganisms were investigated with Folsomia candida – the Drosophila of soil zoologists (Thimm et al., 1998). Depending on the moulting stage of the springtail, numbers of heterotrophic, aerobic gut bacteria, feeding on various substrates, could alter two fold. F. candida preferred to feed on Pseudomonas putida. Ratios of ingested to released bacterial cells demonstrated that populations of nonindigenous gut bacteria like Sinorhizobiummeliloti and E. coli were present. The work demonstrated that F. candida changes its taste for certain bacteria.

Symbiosis between a springtail, Folsomia, and abundant chitin-degrading bacteria, Xanthomonas maltophilia and Curtobacterium sp. enabled it to digest chitin (Borkott & Insam 1990). We want a smilar study examining glomalin, as according to CHGPT as of "January 2022, there is no known bacteria specifically documented to digest glomalin".

The bacteria found in springtail guts are predominantly aerobic bacteria. Bacterial endosymbionts in collembolans have been reported since the 1980s. The microbiota of a brown coloured soil-surface-dwelling springtail, Orchesella, was dominated by the families of Rickettsiaceae, Enterobacteriaceae and Comamonadaceae (Bahrndorff et al., 2018) All are gram-negative aerobic nonfermenting bacilli. Pseudomonas and Stenotrophomonas are other groups found in springtail guts and are also strictly aerobic. The Orchesella work is the only study using springtails from nature rather in labs. This study is by no means conclusive but it is indicative that the relations between roots, fungi and springtails are aerobic, although more work on gut bacteria could build a better picture.

Orchesella

'Visual diagram' of hot glomalin research topics (from (Deng et al 2023). Will we see 'glomalisation' in this diagram in a few years time?

Glomalisation

I have just invented this term to describe the mainly aerobic digestive process, that occurs in springtails but also other small arthropods like proturans, and turns 'recalcitrant' glomalin into sugars and smaller units of protein that feed much of the soil metabolism and help stick soil particles together to improve aggregation. From the word glomalin, itself from Glomeromyces fungi, whose name comes from the term ‘glomeruli’ referring to the arbuscules. It echoes the word humification another major soil process, involving an anaerobic digestive process in other small animals like mites, termites, and worms, that produces humus.

"The highest EE(Easily extractable) GRSP protein was under treatment receiving of paddy straw with Aspergillus spp. + Bacillus spp. + Streptomyces spp." (Shrivastava et al 2018).

To me the process explains the 100k of springtails per m2, but many won't have thought about the role of springtails previously.

My proposal is that springtails eat a lot of glomalin and poo out GRSPs, thereby contributing to improving soil health. A lot of work needs to be done to prove this, and most that relates with this is likely to from India and China (Deng et al 2023) . Are these same bacteria in springtail guts? We saw how springtails follow geosmin emitted by Streptomyces. Did/do they carry Streptomyces in their guts and do these help break down the glomalin?
This should be another question for the 'Glomalin Research Gap' (Globalisation page)

Dispersal

“They (Collembola) therefore found their pasture in the Devonian undergrowth and their role for the dispersion of spores. And the colonization of virgin spaces is probable, and must have been exercised in various regions since at the present time, they withstand extreme temperatures from -13 ° to + 38 ° C and they live as well in the tidal zone as at more than 5000 m of altitude“[p63]. What is it about springtails that make them good spore carriers?

The spores of fungi are much larger than those of bacteria. While springtails eat bacterial spores, fungal spores may be too large to pass through their gut..

“This dual aspect of faunal-microbial relationships is fundamental for understanding soil microbial dynamics and co-evolution of these two groups, similarly to the relationships between pollinators and plants” (Potapov et al., 2020)

We should know a lot more about this faunal-microbial relationship to fill in “the important knowledge gaps that include insufficient information on dispersal of fungal propagules other than spores, the role of invertebrates in the dispersal of mycorrhizal fungi, the way in which propagules pass through food webs, and the spatial distances reached by different dispersal mechanisms both horizontally and vertically.” (Vasutova et al., 2019)

“In the presence of the collembolan, Glomus etunicatum took longer to colonize neighbouring plants, but was able to infect at least 30 cm further, illustrating the arthropod's ability to disperse the AM inoculum. Acaulosporadenticulata increased its range by 10 cm in the presence of F. candida, but unlike G. etunicatum, there was no delay in the colonization. In contrast, colonization of neighbouring plants by Scutellosporacalospora (another AM fungi) was negatively affected both in terms of overall distance and time. These data support the hypothesis that soil arthropods can act as dispersal agents for AM inoculum, but the extent of this is fungal species-specific” (Klironomos, 1999)

It appears that, for Collembola, dispersal of fungal propagules is mainly via exterior body parts rather than through the faeces.The soil animal would be opening "pioneer habitats" by soil to allow fungi such as Mortierella and Mucorplaces to avoid competition. (Visser, Parkinson, and Hassall, 2011)

Fungal spores on springtail skin
C055/0624 Rights Managed

How springtails pass on spores as explained by this author in BBC Gardener's World or click the graphic

Spores

Fungal spores stick to creatures accidentally. In particular they could also stick to the sticky organ of springtails – collophore - and are carried with the springtail when it starts nibbling at some root material or fungus growing out of it. This delivers the spore to where it needs to be – on the root, so it can establish that mycorrhizal relationship.

But there are little data to prove AMF dispersing ability of Collembola. In one experiment (Seres, Bakonyi, and Posta, 2007) Folsomia candida did not consume the spores of the AMF Glomus mossea, but Sinella consumed 45% of the G. mossea spores and 71% of another Glomus spores. Both species were able to disperse mycorrhiza in the soil, but the efficiency of dispersal was different. F. candida carried the infection more effectively than S. coeca, in spite of the fact that F. candida did not consume the spores in the food choice experiment. The total plant biomass was 23% higher in the presence of F. candida and 8.5% higher in the presence of S. coeca. Collembola improved the dispersion of the AM fungi, therefore enhanced the nutrient and water uptake of the plant.

Sinella

Sex

Springtails must have one of first creatures on earth showing sexual behaviours. The springtails developed various forms of reproduction, to make the most of the litter environment. Unlike most creatures, it is the male who leaves a spermatophore around (left on stalk) and then the female comes to collect. To encourage that, Ghilarov identifies Endomorphs (top) where males try and attract the females attention, while the Poduran male (left) give the females a nudge and the Sminthurids (bottom right and below) head butt each other.

From Ghilarov 1959

Sminths

Some of the Smithurids have incredible dances. One of the most famous is the courtship dance of Deuterosminthurus pallipes, a mainstay on the sunny leaves of early summer bedding plants across Europe. A receptive female and one or more smaller male suitors will engage in a contest of banging heads and fast spinning until one male is hopefully victorious. He then deposits a drop of sperm which the female will take up. Bear in mind that these globular springtails are all 1mm or smaller.

Other species are more acrobatic, like Stenacidia, Sminthurides and Sphaeridiaspecies, who all participate in a ritual where, after some initial manoeuvring and wooing of the prospective female, the male attaches himself to the female’s antennae, using specialised hooks on his antennae. She then lifts him aloft and eventually he can guide her to the spermatophore, a ‘sperm bag on a stick’, attached to the substrate, which she then accepts and absorbs

But were Sminths around then? Later perhaps.

Living fossils

Charles Darwin coined the term "living fossil" in 1859 to describe living species that still looked like their ancestors from millions of years ago and were often the last surviving lineage. Here the likes of endobryomorphic springtails that running round now look like the ones 400mya. This is remarkable, especially when we remember they must have survived several major ‘extinctions’ during that time. The added curiosity is the big gap between the first springtail fossils and anything remotely related with them before that – say crustacea 100 my previously.

We can talk about their environment then using ‘living fossil’ idea. Their environment then and now must be similar - otherwise they would have changed. That tells us a lot. Most live in the litter layer, under stones, around roots and in moss. So presumably that is what the surface of land looked like then.

In terms of dry springtail biomass, it has recently been found that there is a 20-fold biomass difference between the tundra and the tropics (Popatov et al., 2023). Sampling from nearly 2500 sites found that the are 30X more per m−2 in the tundra than in the tropics. That implies the conditions were probably akin to tundra - treeless, with low growing plants like moss - although some present-day tundra plants would not have been round then - like grasses.

Have collembola stayed a separate entity for 400my as they have a reasonable secure environment? The three (or four) main groups of collembola seem to have originated around the same time. Each group was to evolve in various ways, as we will see.

Phylogeny

Collembola are key taxon when working out relations of arthropods, but this is anything but clear. (Regier 2009) They were classed as insects until the early 1990s when it was deemed their mouthparts nor furcula or collophore fitted in to the insect class.

They have two close relations, proturans which we met earlier and diplurans who we will meet later.

"The main problems are the unclear relationships among the basal hexapod lineages - Entognatous - Protura (proturans), Collembola (springtails), Diplura (diplurans), and Ectognatha (bristletails, silverfishes, and all winged insects" (Sasaki et al., 2013)

The morphology of collembola bears little relationship with crustacea, but the genes match up more closely. In perhaps the most comprehensive review of the origin of springtails, looking at their relations with insects, hexapods, myriapods and crustacea, Collembola are not so-called primitive insects without wings, but a unique and ancient group of well adapted terrestrial crustaceans.”

A Royal Society ‘molecular’ study concluded: “The analyses performed for the 24 different weighting schemes yielded the same conclusion: semi–aquatic ecology is not ancestral for the springtails. It is a derived condition that evolved independently several times. The adaptation for semi-aquatic life is better interpreted as a step towards independence from land, rather than indication of an aquatic origin” (Haese, 2002)

Just 10 years ago, “The phylogenetic relationships among the basal hexapod lineages remain unclear despite the considerable research efforts that have conducted in attempts to resolve them.” (Sasaki et al., 2013)

More recently, "Phylogenetic analyses of single genes and transcriptomes confirm that Hexapoda are a subgroup of Pancrustacea, arguably most closely related with the specialized cave-dwelling Remipedia. The earliest evolutionary history in the marine environment remains unknown. The monophyly of Hexapoda is clearly supported by molecular evidence, by the specific tagmosis, and by morphological apomorphies implied by the Pancrustacea concept. The basal branching pattern, i.e., the interrelationships of the entognathous orders remain ambivalent. The monophyly of Insecta (= Ectognatha), Zygentoma (incl. the “living fossil” Tricholepidion), Dicondylia (= Zygentoma + pterygote insects), and Pterygota is confirmed." (Beutel et al 2017)

Entomobryomorphs

Isotoma

Pogonognathellus

4 Orders

Within Collembola, there has been a debate about relations between the main orders, but “it is nevertheless now widely accepted that four orders of Collembola should be considered: Entomobryomorpha, Neelipleona, Poduromorpha, and Symphypleona (Leo et al., 2019). It looks like the Entomobryomorphs were the predominant order around at this time, and the others came later. They may well have looked very much like this for 400my.

These original surface-dwelling springtails are generally large, have darker pigments, have longer antennae and functioning furca. These larger surface springtails, Endobryomorphs, live in air are generally 8-10 millimeters in length, pigmented, have long limbs, and a full set of photoreceptors. They are also the oldest in evolutionary terms. This was the evolutionary climax for collembola, as later they loose many of these features.

We shall see as we go along how and when the other springtail groups emerged.

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