Abstract
The present knowledge on chemical communication in springtails (Collembola), one of the two most abundant invertebrate groups living in soil and environments in tight contact with soil (e.g. plant litter, moss), is reviewed here. Chemical communication in an environment where light is absent or dimmed becomes a prominent driver of trophic and non-trophic interactions between soil organisms at a time when better knowledge on the biological determinants of soil communities is required. Like insects and many other arthropods, collembolan individuals of the same population intercommunicate by pheromones, which allow them signalling a risk or clustering in places favourable for feeding, mating, moulting and ovipositing. Olfaction is also used to select preferred food and mates. Researches so far conducted allowed discerning common trends in the role and chemical composition of odour blends used by Collembola. However, much more needs to be done before reaching straightforward conclusions about chemical communication issues at evolutionary and community levels, making this domain even more rewarding.
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Change history
22 April 2020
The author regrets at the beginning of the sub-section "Sex pheromones" (page 428 of the published version) within the section "The use of pheromones, allomones and kairomones by Collembola"
References
Altner H, Thies G (1976) The postantennal organ: a specialized unicellular sensory input to the protocerebrum in apterygotan insects (Collembola). Cell Tissue Res 167:97–110
Anderson JM (1975) The enigma of soil animal species diversity. In: Vanek J (ed) Progress in soil zoology. Academia, Prague, pp 51–58
Anderson JM (1978) Competition between two unrelated species of soil Cryptostigmata (Acari) in experimental microcosms. J Anim Ecol 47:787–803
Auclerc A, Ponge JF, Barot S, Dubs F (2009) Experimental assessment of habitat preference and dispersal ability of soil springtails. Soil Biol Biochem 41:1596–1604
Auclerc A, Libourel PA, Salmon S, Bels V, Ponge JF (2010) Assessment of movement patterns in Folsomia candida (Hexapoda: Collembola) in the presence of food. Soil Biol Biochem 42:657–659
Austin AT, Vivanco L, González-Arzac A, Pérez LI (2014) There’s no place like home? An exploration of the mechanisms behind plant litter-decomposer affinity in terrestrial ecosystems. New Phytol 204:307–314
Bahrndorff S, De Jonge N, Hansen JK, Lauritzen JMS, Spanggaard LH, Sorensen MH, Yde M, Nielsen JL (2018) Diversity and metabolic potential of the microbiota associated with a soil arthropod. Sci Report 8:2491
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Baker TC (2002) Mechanism for saltational shifts in pheromone communication systems. Proc Natl Acad Sci U S A 99:13368–13370
Baldock JA, Nelson PN (2000) Soil organic matter. In: Sumner ME et al (eds) Handbook of soil science. CRC Press, Boca Raton, pp B25–B84
Barata EN, Mustaparta H, Pickett JA, Wadhams LJ, Araujo J (2002) Encoding of host and non-host plant odours by receptor neurones in the eucalyptus woodborer, Phoracantha semipunctata (Coleoptera: Cerambycidae). J Comp Physiol A 188:121–133
Bardgett RD (2002) Causes and consequences of biological diversity in soil. Zoology 105:367–374
Bardgett RD, Van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511
Barot S, Gignoux J (2004) Mechanisms promoting plant coexistence: can all the proposed processes be reconciled? Oikos 106:185–192
Barra JA, Christiansen K (1975) Experimental study of aggregations during the development of Pseudosinella impediens (Collembola, Entomobryidae). Pedobiologia 15:343–347
Beck JJ, Alborn HT, Block AK, Christensen SA, Hunter CT, Rering CC, Seidl-Adams I, Stuhl CJ, Torto B, Tumlinson JH (2018) Interactions among plants, insects, and microbes: elucidation of inter-organismal chemical communications in agricultural ecology. J Agric Food Chem 66:6663–6674
Bell WJ, Tobin TR (1982) Chemo-orientation. Biol Rev Cambridge Phil Soc 57:219–260
Bengtsson G, Erlandsson A, Rundgren S (1988) Fungal odour attracts soil Collembola. Soil Biol Biochem 20:25–30
Bengtsson G, Hedlund K, Rundgren S (1991) Selective odor perception in the soil Collembola Onychiurus armatus. J Chem Ecol 17:2113–2125
Bengtsson G, Hedlund K, Rundgren S (1994) Food- and density-dependent dispersal: evidence from a soil collembolan. J Anim Ecol 63:513–520
Benoit JB, Elnitsky MA, Schulte GG, Lee RE Jr, Denlinger DL (2009) Antarctic collembolans use chemical signals to promote aggregation and egg laying. J Insect Behav 22:121–133
Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193
Betsch-Pinot MC (1977) Les parades sexuelles primitives chez les Collemboles Symphypléones. Rev Écol Biol Sol 14:15–19
Biedermann PHW, De Fine Licht HK, Rohlfs M (2019) Evolutionary chemo-ecology of insect-fungus interactions: still in its infancy but advancing. Fungal Ecol 38:1–6
Bitzer C, Brasse G, Dettner K, Schulz S (2004) Benzoic acid derivatives in a hypogastrurid collembolan: temperature-dependent formation and biological significance as deterrents. J Chem Ecol 30:1591–1602
Blomquist GJ, Figueroa-Teran R, Aw M, Song MM, Gorzalski A, Abbott NL, Chang E, Tittiger C (2010) Pheromone production in bark beetles. Insect Biochem Mol Biol 40:699–712
Blouin M, Zuily-Fodil Y, Pham-Thi AT, Laffray D, Reversat G, Pando A, Tondoh J, Lavelle P (2005) Belowground organism activities affect plant aboveground phenotype, inducing plant tolerance to parasites. Ecol Lett 8:202–208
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631
Boulay J, Aubernon C, Ruxton GD, Hédouin V, Deneubourg JL, Charabidzé V (2019) Mixed-species aggregations in arthropods. Insect Sci 26:2–19
Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274
Brückner A, Schuster R, Smit T, Pollierer MM, Schäffler I, Heethoff M (2018) Track the snaff: olfactory cues shape foraging behaviour of decomposing soil mites (Oribatida). Pedobiologia 66:74–80
Callaway RM (2002) The detection of neighbors by plants. Trends Ecol Evol 17:104–105
Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848
Chauvat M, Perez G, Ponge JF (2014) Foraging patterns of soil springtails are impacted by food resources. Appl Soil Ecol 82:72–77
Chernova NM, Potapov MB, Savenkova YY, Bokova AI (2010) Ecological significance of parthenogenesis in Collembola. Entomol Rev 90:23–38
Christiansen K (1967) Competition between collembolan species in culture jars. Rev Écol Biol Sol 4:439–462
Christiansen K, Doyle M, Kahlert M, Gobaleza D (1992) Interspecific interactions between collembolan populations in culture. Pedobiologia 36:274–286
Combès A, Ndoye I, Bance C, Bruzaud J, Djediat C, Dupont J, Nay B, Prado S (2012) Chemical communication between the endophytic fungus Paraconiothyrium variabile and the phytopathogen Fusarium oxysporum. PLoS One 7:e47313
Corey EA, Bobkov Y, Ukhanov K, Ache BW (2013) Ionotropic crustacean olfactory receptors. PLoS One 8:e60551
Croft JR, Liu T, Camiletti AL, Simon AF, Thompson GJ (2017) Sexual response of male Drosophila to honey bee queen mandibular pheromone: implications for generic studies of social insects. J Comp Physiol A 203:143–149
Culver D (1974) Competition between Collembola in a patchy environment. Rev Écol Biol Sol 11:533–540
De Bruyn M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897
De Vries FT, Thébault E, Liiri M, Birkhofer K, Tsiafouli MA, Bjørnlund L, Bracht Jørgensen H, Brady MV, Christensen S, De Ruiter PC, D’Hertefeldt T, Frouz J, Hedlund K, Hemerik L, Hol WHG, Hotes S, Mortimer SR, Setälä H, Sgardelis SP, Uteseny K, Van der Putten WH, Wolters V, Bardgett RD (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci U S A 110:14296−14301
DeAngelis KM (2016) Chemical communication connects soil food webs. Soil Biol Biochem 102:48–51
Dettner K, Scheuerlein A, Fabian P, Schulz S, Francke W (1996) Chemical defense of giant springtail Tetrodotonphora bielanensis (Waga) (Insecta: Collembola). J Chem Ecol 22:1051–1074
Dickschat JS, Reichenbach H, Wagner-Dobler I, Schulz S (2005) Novel pyrazines from the myxobacterium Chondromyces crocatus and marine bacteria. Eur J Org Chem 2005:4141–4153
Dillon R, Charnley K (2002) Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res Microbiol 153:503–509
Dugdale JS (1997) Pheromone and morphology-based phylogenies in New Zealand tortricid moths. In: Carde RT, Minks AK (eds) Insect pheromone research: new directions. Chapman and Hall, London, pp 463–472
Eijsackers H (1978) Side effects of the herbicide 2,4,5-T affecting mobility and mortality of the springtail Onychiurus quadriocellatus Gisin (Collembola). Z Angew Entomol 86:349–372
Ferlian O, Klarner B, Langeneckert AE, Scheu S (2015) Trophic niche differentiation and utilisation of food resources in collembolans based on complementary analyses of fatty acids and stable isotopes. Soil Biol Biochem 82:28–35
Futuyma DJ, Mitter C (1996) Insect-plant interactions: the evolution of component communities. Phil Trans R Soc London B 351:1361–1366
Gerson U (1969) Moss-arthropod associations. Bryologist 72:495–500
Giribet G, Edgecombe GD, Carpenter JM, D’Haese C, Wheeler WC (2004) Is Ellipura monophyletic? A combined analysis of basal hexapod relationships with emphasis on the origin of insects. Org Divers Evol 4:319–340
Glasgow JP (1939) A population study of subterranean soil Collembola. J Anim Ecol 8:323–353
Gould SJ, Eldredge N (1993) Punctuated equilibrium comes of age. Nature 366:223–227
Greenfield MD (1981) Moth sex pheromones: an evolutionary perspective. Florida Entomol 64:4–17
Greenway AR, Griffiths DC, Lloyd SL (1978) Response of Myzus persicae to components of aphid extracts and to carboxylic acids. Entomol Exp Appl 24:369–374
Hale WG (1966) A population study of moorland Collembola. Pedobiologia 6:65–99
Hayashi M, Nakamura Y, Higashi K, Kato H, Kishida F, Kaneko H (1999) A quantitative structure-activity relationship study of the skin irritation potential of phenols. Toxicol in Vitro 13:915–922
Heděnec P, Radochová P, Nováková A, Kaneda S, Frouz J (2013) Grazing preference and utilization of soil fungi by Folsomia candida (Isotomidae: Collembola). Eur J Soil Biol 55:66–70
Hedlund K, Ek H, Gunnarsson T, Svegborn C (1990) Mate choice and male competition in Orchesella cincta (Collembola). Experientia 46:524–526
Hedlund K, Bengtsson G, Rundgren S (1995) Fungal odour discrimination in two sympatric species of fungivorous collembolans. Funct Ecol 9:869–875
Hopkin SP (1997) Biology of the springtails (Insecta: Collembola). Oxford University Press, Oxford
Howard RW, Blomquist GJ (1982) Chemical ecology and biochemistry of insect hydrocarbons. Annu Rev Entomol 27:149–172
Huber I (1978) Prey attraction and immobilization by allomone from nymphs of Womersia strandtmanni (Acarina: Trombiculidae). Acarologia 20:112–115
Ims RA, Leinaas HP, Coulson S (2004) Spatial and temporal variation in patch occupancy and population density in a model system of an arctic Collembola species assemblage. Oikos 105:89–100
Ishii S, Kuwahara Y (1967) An aggregation pheromone of the German cockroach Blatella germanica L. (Orthoptera: Blatellidae). I. Site of the pheromone production. Appl Entomol Zool 2:203–217
Joosse ENG (1970) The formation and biological significance of aggregations in the distribution of Collembola. Netherl J Zool 20:299–314
Joosse ENG (1971) Ecological aspects of aggregation in Collembola. Rev Écol Biol Sol 8:91–97
Joosse ENG, Koelman TACM (1979) Evidence for the presence of aggregation pheromones in Onychiurus armatus (Collembola), a pest insect in sugar beet. Entomol Exp Appl 26:197–201
Joosse ENG, Verhoef HA (1974) On the aggregational habits of surface dwelling Collembola. Pedobiologia 14:245–249
Jørgensen HB, Johansson T, Canbäck B, Hedlund K, Tunlid A (2005) Selective foraging of fungi by collembolans in soil. Biol Lett 1:243–246
Jousset A, Scheu S, Bonkowski M (2008) Secondary metabolite production facilitates establishment of rhizobacteria by reducing both protozoan predation and the competitive effects of indigenous bacteria. Funct Ecol 2008:714–719
Kaissling KE (2014) Pheromone reception in insects: the example of silk moths. In: Mucignat-Caretta C (ed) Neurobiology of chemical communication. CRC Press, Boca Raton, FL, pp 99–146
Karlson P, Luscher M (1959) Pheromones: new term for a class of biologically active substances. Nature 183:55–56
Karuhize GR (1971) The structure of the postantennal organ in Onychiurus sp. (Insecta: Collembola) and its connection to the central nervous system. Z Zellforsch Mikroskop Anatomie 118:263–282
Keil TA (1999) Morphology and development of the peripheral olfactory organs. In: Hansson BS (ed) Insect olfaction. Springer Nature, Stuttgart, pp 5–47
Kielty JP, Allen-Williams LJ, Underwood N, Eastwood EA (1996) Behavioral responses of three species of ground beetle (Coleoptera: Carabidae) to olfactory cues associated with prey and habitat. J Insect Behav 9:237–250
Knight CB, Angel RA (1967) A preliminary study of the dietary requirements of Tomocerus (Collembola). Am Midl Nat 77:510–517
Kollmann M, Huetteroth W, Schachtner J (2011) Brain organization in Collembola (springtails). Arthropod Struct Develop 40:304–316
Kozlowski MW, Shi AX (2006) Ritual behaviors associated with spermatophore transfer in Deuterosminthurus bicinctus (Collembola: Bourletiellidae). J Ethol 24:103–109
Krool S, Bauer T (1987) Reproduction, development, pheromone secretion in Heteromurus nitidus Templeton 1835 (Collembola, Entomobryidae). Rev Écol Biol Sol 24:187–195
Kuenen DJ, Nooteboom HP (1963) Olfactory orientation in some land-isopods (Oniscoidea, Crustacea). Entomol Exp Appl 6:133–142
Laland KN, Boogert NJ (2010) Niche construction, co-evolution and biodiversity. Ecol Econ 69:731–736
Lavelle P, Spain A, Blouin M, Brown G, Decaëns T, Grimaldi M, Jiménez JJ, McKey D, Mathieu J, Velasquez E, Zangerlé A (2016) Ecosystem engineers in a self-organized soil: a review of concepts and future research questions. Soil Sci 181:91–109
Leach JE, Triplett LR, Argueso CT, Trivedi P (2017) Communication in the phytobiome. Cell 169:587–596
Leal WS (1997) Evolution of sex pheromone communication in plant-feeding scarab beetles. In: Carde RT, Minks AK (eds) Insect pheromone research: new directions. Chapman and Hall, London, pp 505–513
Lei H, Chiu HY, Hildebrand JG (2013) Responses of protocerebral neurons in Manduca sexta to sex-pheromone mixtures. J Comp Physiol A 199:997–1014
Leigh EG Jr, Rowell TE (1995) The evolution of mutualism and other forms of harmony at various levels of biological organization. Ecologie 26:131–158
Leinaas HP (1983) Synchronized moulting controlled by communication in group-living Collembola. Science 219:193–195
Leonard MA, Bradbury PC (1984) Aggregative behaviour in Folsomia candida (Collembola: Isotomidae), with respect to previous conditioning. Pedobiologia 26:369–372
Liu J, Wu DH (2017) Chemical attraction of conspecifics in Folsomia candida (Collembola). J Insect Behav 30:331–341
Lyford WH (1975) Overland migration of Collembola (Hypogastrura nivicola Fitch) colonies. Am Midl Nat 94:205–209
Malcicka M, Ruther J, Ellers J (2017) De novo synthesis of linoleic acid in multiple Collembola species. J Chem Ecol 43:911–919
Malcicka M, Visser B, Ellers J (2018) An evolutionary perspective on linoleic acid synthesis in animals. Evol Biol 45:15–26
Manica A, McMeechan FK, Foster WA (2001) An aggregation pheromone in the intertidal collembolan Anurida maritima. Entomol Exp Appl 99:393–395
Maraun M, Martens H, Migge S, Theenhaus A, Scheu S (2003) Adding to the ‘enigma of soil animal diversity’: fungal feeders and saprophagous soil invertebrates prefer similar food substrates. Eur J Soil Biol 39:85–95
Marseille F, Disnar JR, Guillet B, Noack Y (1999) n-Alkanes and free fatty acids in humus and A1 horizons of soils under beech, spruce and grass in the Massif-Central (Mont-Lozère), France. Eur J Soil Sci 50:433–431
Mendelson TC, Martin MD, Flaxman S (2014) Mutation-order divergence by sexual selection: diversification of sexual signals in similar environments as a first step in speciation. Ecol Lett 17:1053–1066
Mertens J, Bourgoignie R (1977) Aggregation pheromone in Hypogastrura viatica (Collembola). Behav Ecol Sociobiol 2:41–48
Mertens J, Blancquaert JP, Bougoignie R (1979) Aggregation pheromone in Orchesella cincta (Collembola). Rev Écol Biol Sol 16:441–447
Messer C, Dettner K, Schulz S, Francke W (1999) Phenolic compounds in Neanura muscorum (Collembola, Neanuridae) and the role of 1,3-dimethoxybenzene as an alarm substance. Pedobiologia 43:174–182
Michelozzi M, Raschi A, Tognetti R, Tosi L (1997) Eco-ethological analysis of the interaction between isoprene and the behaviour of Collembola. Pedobiologia 41:210–214
Missbach C, Dweck HKM, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, Grosse-Wilde E (2014) Evolution of insect olfactory receptors. eLIFE 3:e02115
Negri I (2004) Spatial distribution of Collembola in presence and absence of a predator. Pedobiologia 48:585–588
Nijholt WW (1980) Pine oil and oleic acid delay and reduce attacks on logs by ambrosia beetles (Coleoptera: Scolytidae). Can Entomol 112:199–204
Nilsson E, Bengtsson G (2004a) Death odour changes movement pattern of a Collembola. Oikos 104:509–517
Nilsson E, Bengtsson G (2004b) Endogenous free fatty acids repel and attract Collembola. J Chem Ecol 30:1431–1443
O’Connell RJ (1986) Chemical communication in invertebrates. Experientia 42:232–241
Perez G, Aubert M, Decaëns T, Trap J, Chauvat M (2013) Home-field advantage: a matter of interaction between litter biochemistry and decomposer biota. Soil Biol Biochem 67:245–254
Peters NK, Verma DPS (1990) Phenolic compounds as regulators of gene expression in plant-microbe interactions. Mol Plant-Microb Interact 3:4–8
Pfander I, Zettel J (2004) Chemical communication in Ceratophysella sigillata (Collembola: Hypogastruridae): intraspecific reaction to alarm substances. Pedobiologia 48:575–580
Ponge JF (1973) Application de l’analyse factorielle des correspondances à l’étude des variations annuelles dans les populations de microarthropodes. Bull Ecol 4:319–327
Ponge JF (2000) Vertical distribution of Collembola (Hexapoda) and their food resources in organic horizons of beech forests. Biol Fertil Soils 32:508–522
Ponge JF, Salmon S (2013) Spatial and taxonomic correlates of species and species trait assemblages in soil invertebrate communities. Pedobiologia 56:129–136
Poole TB (1961) An ecological study of the Collembola in a coniferous forest soil. Pedobiologia 1:113–137
Porco D, Deharveng L, Gers C (2004) Sexual discrimination with cuticular lipids in Schoetella ununguiculata (Tullberg, 1869) (Collembola: Hypogastruridae). Pedobiologia 48:581–583
Porco D, Deharveng L, Skarżyński D (2009) Sex pheromone in Tetrodontophora bielanensis (Waga, 1842) (Collembola: Onychiuridae): indirect reproduction mediated by cuticular compounds. Pedobiologia 53:59–63
Prinzing A, Ozinga WA, Brändle M, Courty PE, Hennion F, Labandeira C, Parisod C, Pihain M, Bartish IV (2017) Benefits from living together? Clades whose species use similar habitats may persist as a result of eco-evolutionary feedbacks. New Phytol 213:66–82
Puga-Freitas R, Blouin M (2015) A review of the effects of soil organisms on plant hormone signalling pathways. Environ Exp Bot 114:104–116
Purrington FF, Kendall PA, Bater JE, Stinner BR (1991) Alarm pheromone in a gregarious poduromorph collembolan (Collembola: Hypogastruridae). Great Lakes Entomol 24:75–78
Reddy GVP, Guerrero A (2004) Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci 9:253–261
Reiffarth EL, Petticrew PN, Owens DA Lobb DG (2016) Sources of variability in fatty acid (FA) biomarkers in the application of compound-specific stable isotopes (CSSIs) to soil and sediment fingerprinting and tracing: a review. Sci Total Environ 565:8–27
Roelofs WL, Brown RL (1982) Pheromones and evolutionary relationships of Tortricidae. Annu Rev Ecol Syst 13:395–422
Rollo CD, Czyzewska E, Borden JH (1994) Fatty acid necromones for cockroaches. Naturwissenschaften 81:409–410
Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. mBio 7:e01395–e01315
Rosenstiel TN, Shortlidge EE, Melnychenko AN, Pankow JF, Eppley SM (2012) Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss. Nature 489:431–433
Sadaka-Laulan N, Ponge JF, Roquebert MF, Bury É, Boumezzough A (1998) Feeding preferences of the collembolan Onychiurus sinensis for fungi colonizing holm oak litter (Quercus rotundifolia Lam.). Eur J Soil Biol 34:179–188
Salmon S (2001) Earthworm excreta (mucus and urine) affect the distribution of springtails in forest soils. Biol Fertil Soils 34:304–310
Salmon S (2004) The impact of earthworms on the abundance of Collembola: improvement of food resources or of habitat? Biol Fertil Soils 40:323–333
Salmon S, Ponge JF (1999) Distribution of Heteromurus nitidus (Hexapoda, Collembola) according to soil acidity: interactions with earthworms and predator pressure. Soil Biol Biochem 31:1161–1170
Salmon S, Ponge JF (2001) Earthworm excreta attract soil springtails: laboratory experiments on Heteromurus nitidus (Collembola: Entomobryidae). Soil Biol Biochem 33:1959–1969
Salmon S, Geoffroy JJ, Ponge JF (2005) Earthworms and Collembola relationships: effects of predatory centipedes and humus forms. Soil Biol Biochem 37:487–495
Sánchez-García A, Peñalver E, Delclòs X, Engel MS (2018) Mating and aggregative behaviors among basal hexapods in the Early Cretaceous. PLoS One 13:e0191669
Sanon A, Andrianjaka ZN, Prin Y, Bally R, Thioulouse J, Comte G, Duponnois R (2009) Rhizosphere microbiota interferes with plant-plant interactions. Plant Soil 321:259–278
Sbarbati A, Osculati F (2006) Allelochemical communication in vertebrates: kairomones, allomones and synomones. Cells Tissues Organs 183:206–219
Schooley RL, Wiens JA (2003) Finding habitat patches and directional connectivity. Oikos 102:559–570
Seastedt TR (1984) The role of microarthropods in decomposition and mineralization process. Annu Rev Entomol 29:25–46
Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E (2013) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci U S A 110:4853–4853
Shorey HH (1973) Behavioural responses to insect pheromones. Annu Rev Entomol 18:349–380
Smolanoff J, Kluge AF, Meinwald J, McPhail A, Miller RW, Hicks K, Eisner T (1975) Polyzonimine: a novel terpenoid insect repellent produced by a millipede. Science 188:734–736
Staaden S, Milcu A, Rohlfs M, Scheu S (2011) Olfactory cues associated with fungal grazing intensity and secondary metabolite pathway modulate Collembola foraging behaviour. Soil Biol Biochem 43:1411–1416
Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. BioScience 51:235–246
Stam E, Isaaks A, Ernsting G (2002) Distant lovers: spermatophore deposition and destruction behaviour by male springtails. J Insect Behav 15:253–268
Stamps JA, Swaisgood RR (2007) Someplace like home: experience, habitat selection and conservation biology. Appl Anim Behav Sci 102:392–409
Stökl J, Steiger S (2017) Evolutionary origin of insect pheromones. Curr Opinion Insect Sci 24:36–42
Stötefeld L, Scheu S, Rohlfs M (2012) Fungal chemical defence alters density-dependent foraging behaviour and success in a fungivorous soil arthropod. Ecol Entomol 37:323–329
Symonds MRE, Elgar MA (2004) The mode of pheromone evolution: evidence from bark beetles. Proc R Soc Lond B 271:839–846
Symonds MRE, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228
Symonds MRE, Wertheim B (2005) The mode of evolution of aggregation pheromones in Drosophila species. J Evol Biol 18:1253–1263
Taga ME, Bassler BL (2003) Chemical communication among bacteria. Proc Natl Acad Sci U S A 100:14549–14554
Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ (1999) Insect pheromones: an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol 29:481–514
Usher MB (1969) Some properties of the aggregations of soil arthropods: Collembola. J Anim Ecol 38:607–622
Usher MB, Balogun RA (1966) A defence mechanism in Onychiurus (Collembola, Onychiuridae). Entomol Monthly Mag 102:237–238
Van Arnam EB, Currie CR, Clardy J (2018) Defense contracts: molecular protection in insect-microbe symbioses. Chem Soc Rev 47:1638–1651
Veen GF, Freschet GT, Ordonez A, Wardle DA (2015) Litter quality and environmental controls of home-field advantage effects on litter decomposition. Oikos 124:187–195
Verhoef HA (1984) Releaser and primer pheromones in Collembola. J Insect Physiol 30:665–670
Verhoef HA, Nagelkerke CJ (1977) Formation and ecological significance of aggregations of Collembola. Oecologia 31:215–226
Verhoef HA, Nagelkerke CJ, Joosse ENG (1977a) Aggregation pheromones in Collembola. J Insect Physiol 23:1009–1013
Verhoef HA, Nagelkerke CJ, Joosse ENG (1977b) Aggregation pheromones in Collembola (Apterygota): a biotic cause of aggregation. Rev Écol Biol Sol 14:21–25
Vet LEM (1999) From chemical to population ecology: infochemical use in an evolutionary context. J Chem Ecol 25:31–49
Waldorf ES (1974a) Sex pheromone in the springtail, Sinella curviseta. Environ Entomol 3:916–918
Waldorf ES (1974b) Variations in cleaning between the sexes of Sinella coeca (Collembola: Entomobryidae). Psyche 81:254–257
Waldorf ES (1976) Antennal amputation in Sinella curviseta (Collembola: Entomobryidae). Ann Entomol Soc Am 69:841–842
Wall DH, Moore JC (1999) Interactions underground: soil biodiversity, mutualism, and ecosystem processes. BioScience 49:109–117
Walsh MI, Bolger T (1993) Effects of diet on the interactions between Hypogastrura denticulata Bagnall and Onychiurus furcifer Börner in laboratory cultures. Eur J Soil Biol 29:155–160
Wehner K, Norton RA, Blüthgen N, Heethoff M (2016) Specialization of Oribatid mites to forest microhabitats: the enigmatic role of litter. Ecosphere 7:e01336
Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506
Wertheim B, Van Baalen EJA, Dicke M, Vet LEM (2005) Pheromone-mediated aggregation in non-social arthropods: an evolutionary ecological perspective. Annu Rev Entomol 50:321–346
Westerberg L, Lindström T, Nilsson E, Wennergren U (2008) The effect on dispersal from complex correlations in small-scale movement. Ecol Model 213:263–272
Widenfalk LA, Malmström A, Berg MP, Bengtsson J (2016) Small-scale Collembola community composition in a pine forest soil: overdispersion in functional traits indicates the importance of species interactions. Soil Biol Biochem 103:52–62
Wilson EO, Bossert WH (1963) Chemical communication among animals. Recent Prog Horm Res 19:673–716
Wisz MS, Pottier J, Kissling WD, Pellissier L, Lenoir J, Damgaard CF, Dormann CF, Forchhammer MC, Grytnes JA, Guisan A, Heikkinen RK, Høye TT, Kühn I, Luoto M, Maiorano L, Nilsson MC, Normand S, Öckinger E, Schmidt NM, Termansen M, Timmermann A, Wardle DA, Aastrup P, Svenning JC (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biol Rev 88:15–30
Zhao C, Griffin JN, Wu XW, Sun SC (2013) Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. J Anim Ecol 82:749–758
Zizzari ZV, Braakhuis A, Van Straalen NM, Ellers J (2009) Female preference and fitness benefits of mate choice in a species with dissociated sperm transfer. Anim Behav 78:1261–1267
Zizzari ZV, Engl T, Lorenz S, Van Straalen NM, Ellers J, Groot AT (2017) Love at first sniff: a spermatophore-associated pheromone mediates partner attraction in a collembolan species. Anim Behav 124:221–227
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Salmon, S., Rebuffat, S., Prado, S. et al. Chemical communication in springtails: a review of facts and perspectives. Biol Fertil Soils 55, 425–438 (2019). https://doi.org/10.1007/s00374-019-01365-8
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DOI: https://doi.org/10.1007/s00374-019-01365-8