Biology and Fertility of Soils

, Volume 55, Issue 5, pp 425–438 | Cite as

Chemical communication in springtails: a review of facts and perspectives

  • Sandrine Salmon
  • Sylvie Rebuffat
  • Soizic Prado
  • Michel Sablier
  • Cyrille D’Haese
  • Jian-Sheng Sun
  • Jean-François PongeEmail author


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.


Chemical communication Collembola Pheromones Aggregation Phylogeny Community 



  1. Altner H, Thies G (1976) The postantennal organ: a specialized unicellular sensory input to the protocerebrum in apterygotan insects (Collembola). Cell Tissue Res 167:97–110Google Scholar
  2. Anderson JM (1975) The enigma of soil animal species diversity. In: Vanek J (ed) Progress in soil zoology. Academia, Prague, pp 51–58Google Scholar
  3. Anderson JM (1978) Competition between two unrelated species of soil Cryptostigmata (Acari) in experimental microcosms. J Anim Ecol 47:787–803Google Scholar
  4. Auclerc A, Ponge JF, Barot S, Dubs F (2009) Experimental assessment of habitat preference and dispersal ability of soil springtails. Soil Biol Biochem 41:1596–1604Google Scholar
  5. 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 42:657–659Google Scholar
  6. 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 204:307–314Google Scholar
  7. 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 8:2491Google Scholar
  8. 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 57:233–266Google Scholar
  9. Baker TC (2002) Mechanism for saltational shifts in pheromone communication systems. Proc Natl Acad Sci U S A 99:13368–13370Google Scholar
  10. Baldock JA, Nelson PN (2000) Soil organic matter. In: Sumner ME et al (eds) Handbook of soil science. CRC Press, Boca Raton, pp B25–B84Google Scholar
  11. 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 188:121–133Google Scholar
  12. Bardgett RD (2002) Causes and consequences of biological diversity in soil. Zoology 105:367–374Google Scholar
  13. Bardgett RD, Van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511Google Scholar
  14. Barot S, Gignoux J (2004) Mechanisms promoting plant coexistence: can all the proposed processes be reconciled? Oikos 106:185–192Google Scholar
  15. Barra JA, Christiansen K (1975) Experimental study of aggregations during the development of Pseudosinella impediens (Collembola, Entomobryidae). Pedobiologia 15:343–347Google Scholar
  16. 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 66:6663–6674Google Scholar
  17. Bell WJ, Tobin TR (1982) Chemo-orientation. Biol Rev Cambridge Phil Soc 57:219–260Google Scholar
  18. Bengtsson G, Erlandsson A, Rundgren S (1988) Fungal odour attracts soil Collembola. Soil Biol Biochem 20:25–30Google Scholar
  19. Bengtsson G, Hedlund K, Rundgren S (1991) Selective odor perception in the soil Collembola Onychiurus armatus. J Chem Ecol 17:2113–2125Google Scholar
  20. Bengtsson G, Hedlund K, Rundgren S (1994) Food- and density-dependent dispersal: evidence from a soil collembolan. J Anim Ecol 63:513–520Google Scholar
  21. 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 22:121–133Google Scholar
  22. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193Google Scholar
  23. Betsch-Pinot MC (1977) Les parades sexuelles primitives chez les Collemboles Symphypléones. Rev Écol Biol Sol 14:15–19Google Scholar
  24. Biedermann PHW, De Fine Licht HK, Rohlfs M (2019) Evolutionary chemo-ecology of insect-fungus interactions: still in its infancy but advancing. Fungal Ecol 38:1–6Google Scholar
  25. 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 30:1591–1602Google Scholar
  26. 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 40:699–712Google Scholar
  27. 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 8:202–208Google Scholar
  28. Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631Google Scholar
  29. Boulay J, Aubernon C, Ruxton GD, Hédouin V, Deneubourg JL, Charabidzé V (2019) Mixed-species aggregations in arthropods. Insect Sci 26:2–19Google Scholar
  30. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274Google Scholar
  31. 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 66:74–80Google Scholar
  32. Callaway RM (2002) The detection of neighbors by plants. Trends Ecol Evol 17:104–105Google Scholar
  33. 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 417:844–848Google Scholar
  34. Chauvat M, Perez G, Ponge JF (2014) Foraging patterns of soil springtails are impacted by food resources. Appl Soil Ecol 82:72–77Google Scholar
  35. Chernova NM, Potapov MB, Savenkova YY, Bokova AI (2010) Ecological significance of parthenogenesis in Collembola. Entomol Rev 90:23–38Google Scholar
  36. Christiansen K (1967) Competition between collembolan species in culture jars. Rev Écol Biol Sol 4:439–462Google Scholar
  37. Christiansen K, Doyle M, Kahlert M, Gobaleza D (1992) Interspecific interactions between collembolan populations in culture. Pedobiologia 36:274–286Google Scholar
  38. 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:e47313Google Scholar
  39. Corey EA, Bobkov Y, Ukhanov K, Ache BW (2013) Ionotropic crustacean olfactory receptors. PLoS One 8:e60551Google Scholar
  40. 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 203:143–149Google Scholar
  41. Culver D (1974) Competition between Collembola in a patchy environment. Rev Écol Biol Sol 11:533–540Google Scholar
  42. De Bruyn M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897Google Scholar
  43. 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 110:14296−14301Google Scholar
  44. DeAngelis KM (2016) Chemical communication connects soil food webs. Soil Biol Biochem 102:48–51Google Scholar
  45. Dettner K, Scheuerlein A, Fabian P, Schulz S, Francke W (1996) Chemical defense of giant springtail Tetrodotonphora bielanensis (Waga) (Insecta: Collembola). J Chem Ecol 22:1051–1074Google Scholar
  46. Dickschat JS, Reichenbach H, Wagner-Dobler I, Schulz S (2005) Novel pyrazines from the myxobacterium Chondromyces crocatus and marine bacteria. Eur J Org Chem 2005:4141–4153Google Scholar
  47. Dillon R, Charnley K (2002) Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res Microbiol 153:503–509Google Scholar
  48. 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 463–472Google Scholar
  49. 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 86:349–372Google Scholar
  50. 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 82:28–35Google Scholar
  51. Futuyma DJ, Mitter C (1996) Insect-plant interactions: the evolution of component communities. Phil Trans R Soc London B 351:1361–1366Google Scholar
  52. Gerson U (1969) Moss-arthropod associations. Bryologist 72:495–500Google Scholar
  53. 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 4:319–340Google Scholar
  54. Glasgow JP (1939) A population study of subterranean soil Collembola. J Anim Ecol 8:323–353Google Scholar
  55. Gould SJ, Eldredge N (1993) Punctuated equilibrium comes of age. Nature 366:223–227Google Scholar
  56. Greenfield MD (1981) Moth sex pheromones: an evolutionary perspective. Florida Entomol 64:4–17Google Scholar
  57. Greenway AR, Griffiths DC, Lloyd SL (1978) Response of Myzus persicae to components of aphid extracts and to carboxylic acids. Entomol Exp Appl 24:369–374Google Scholar
  58. Hale WG (1966) A population study of moorland Collembola. Pedobiologia 6:65–99Google Scholar
  59. 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 13:915–922Google Scholar
  60. 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 55:66–70Google Scholar
  61. Hedlund K, Ek H, Gunnarsson T, Svegborn C (1990) Mate choice and male competition in Orchesella cincta (Collembola). Experientia 46:524–526Google Scholar
  62. Hedlund K, Bengtsson G, Rundgren S (1995) Fungal odour discrimination in two sympatric species of fungivorous collembolans. Funct Ecol 9:869–875Google Scholar
  63. Hopkin SP (1997) Biology of the springtails (Insecta: Collembola). Oxford University Press, OxfordGoogle Scholar
  64. Howard RW, Blomquist GJ (1982) Chemical ecology and biochemistry of insect hydrocarbons. Annu Rev Entomol 27:149–172Google Scholar
  65. Huber I (1978) Prey attraction and immobilization by allomone from nymphs of Womersia strandtmanni (Acarina: Trombiculidae). Acarologia 20:112–115Google Scholar
  66. 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 105:89–100Google Scholar
  67. 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 2:203–217Google Scholar
  68. Joosse ENG (1970) The formation and biological significance of aggregations in the distribution of Collembola. Netherl J Zool 20:299–314Google Scholar
  69. Joosse ENG (1971) Ecological aspects of aggregation in Collembola. Rev Écol Biol Sol 8:91–97Google Scholar
  70. 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 26:197–201Google Scholar
  71. Joosse ENG, Verhoef HA (1974) On the aggregational habits of surface dwelling Collembola. Pedobiologia 14:245–249Google Scholar
  72. Jørgensen HB, Johansson T, Canbäck B, Hedlund K, Tunlid A (2005) Selective foraging of fungi by collembolans in soil. Biol Lett 1:243–246Google Scholar
  73. 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 2008:714–719Google Scholar
  74. 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 99–146Google Scholar
  75. Karlson P, Luscher M (1959) Pheromones: new term for a class of biologically active substances. Nature 183:55–56Google Scholar
  76. 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 118:263–282Google Scholar
  77. Keil TA (1999) Morphology and development of the peripheral olfactory organs. In: Hansson BS (ed) Insect olfaction. Springer Nature, Stuttgart, pp 5–47Google Scholar
  78. 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 9:237–250Google Scholar
  79. Knight CB, Angel RA (1967) A preliminary study of the dietary requirements of Tomocerus (Collembola). Am Midl Nat 77:510–517Google Scholar
  80. Kollmann M, Huetteroth W, Schachtner J (2011) Brain organization in Collembola (springtails). Arthropod Struct Develop 40:304–316Google Scholar
  81. Kozlowski MW, Shi AX (2006) Ritual behaviors associated with spermatophore transfer in Deuterosminthurus bicinctus (Collembola: Bourletiellidae). J Ethol 24:103–109Google Scholar
  82. Krool S, Bauer T (1987) Reproduction, development, pheromone secretion in Heteromurus nitidus Templeton 1835 (Collembola, Entomobryidae). Rev Écol Biol Sol 24:187–195Google Scholar
  83. Kuenen DJ, Nooteboom HP (1963) Olfactory orientation in some land-isopods (Oniscoidea, Crustacea). Entomol Exp Appl 6:133–142Google Scholar
  84. Laland KN, Boogert NJ (2010) Niche construction, co-evolution and biodiversity. Ecol Econ 69:731–736Google Scholar
  85. 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 181:91–109Google Scholar
  86. Leach JE, Triplett LR, Argueso CT, Trivedi P (2017) Communication in the phytobiome. Cell 169:587–596Google Scholar
  87. 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 505–513Google Scholar
  88. Lei H, Chiu HY, Hildebrand JG (2013) Responses of protocerebral neurons in Manduca sexta to sex-pheromone mixtures. J Comp Physiol A 199:997–1014Google Scholar
  89. Leigh EG Jr, Rowell TE (1995) The evolution of mutualism and other forms of harmony at various levels of biological organization. Ecologie 26:131–158Google Scholar
  90. Leinaas HP (1983) Synchronized moulting controlled by communication in group-living Collembola. Science 219:193–195Google Scholar
  91. Leonard MA, Bradbury PC (1984) Aggregative behaviour in Folsomia candida (Collembola: Isotomidae), with respect to previous conditioning. Pedobiologia 26:369–372Google Scholar
  92. Liu J, Wu DH (2017) Chemical attraction of conspecifics in Folsomia candida (Collembola). J Insect Behav 30:331–341Google Scholar
  93. Lyford WH (1975) Overland migration of Collembola (Hypogastrura nivicola Fitch) colonies. Am Midl Nat 94:205–209Google Scholar
  94. Malcicka M, Ruther J, Ellers J (2017) De novo synthesis of linoleic acid in multiple Collembola species. J Chem Ecol 43:911–919Google Scholar
  95. Malcicka M, Visser B, Ellers J (2018) An evolutionary perspective on linoleic acid synthesis in animals. Evol Biol 45:15–26Google Scholar
  96. Manica A, McMeechan FK, Foster WA (2001) An aggregation pheromone in the intertidal collembolan Anurida maritima. Entomol Exp Appl 99:393–395Google Scholar
  97. 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 39:85–95Google Scholar
  98. 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 50:433–431Google Scholar
  99. 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 17:1053–1066Google Scholar
  100. Mertens J, Bourgoignie R (1977) Aggregation pheromone in Hypogastrura viatica (Collembola). Behav Ecol Sociobiol 2:41–48Google Scholar
  101. Mertens J, Blancquaert JP, Bougoignie R (1979) Aggregation pheromone in Orchesella cincta (Collembola). Rev Écol Biol Sol 16:441–447Google Scholar
  102. 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 43:174–182Google Scholar
  103. Michelozzi M, Raschi A, Tognetti R, Tosi L (1997) Eco-ethological analysis of the interaction between isoprene and the behaviour of Collembola. Pedobiologia 41:210–214Google Scholar
  104. Missbach C, Dweck HKM, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, Grosse-Wilde E (2014) Evolution of insect olfactory receptors. eLIFE 3:e02115Google Scholar
  105. Negri I (2004) Spatial distribution of Collembola in presence and absence of a predator. Pedobiologia 48:585–588Google Scholar
  106. Nijholt WW (1980) Pine oil and oleic acid delay and reduce attacks on logs by ambrosia beetles (Coleoptera: Scolytidae). Can Entomol 112:199–204Google Scholar
  107. Nilsson E, Bengtsson G (2004a) Death odour changes movement pattern of a Collembola. Oikos 104:509–517Google Scholar
  108. Nilsson E, Bengtsson G (2004b) Endogenous free fatty acids repel and attract Collembola. J Chem Ecol 30:1431–1443Google Scholar
  109. O’Connell RJ (1986) Chemical communication in invertebrates. Experientia 42:232–241Google Scholar
  110. 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 67:245–254Google Scholar
  111. Peters NK, Verma DPS (1990) Phenolic compounds as regulators of gene expression in plant-microbe interactions. Mol Plant-Microb Interact 3:4–8Google Scholar
  112. Pfander I, Zettel J (2004) Chemical communication in Ceratophysella sigillata (Collembola: Hypogastruridae): intraspecific reaction to alarm substances. Pedobiologia 48:575–580Google Scholar
  113. Ponge JF (1973) Application de l’analyse factorielle des correspondances à l’étude des variations annuelles dans les populations de microarthropodes. Bull Ecol 4:319–327Google Scholar
  114. Ponge JF (2000) Vertical distribution of Collembola (Hexapoda) and their food resources in organic horizons of beech forests. Biol Fertil Soils 32:508–522Google Scholar
  115. Ponge JF, Salmon S (2013) Spatial and taxonomic correlates of species and species trait assemblages in soil invertebrate communities. Pedobiologia 56:129–136Google Scholar
  116. Poole TB (1961) An ecological study of the Collembola in a coniferous forest soil. Pedobiologia 1:113–137Google Scholar
  117. Porco D, Deharveng L, Gers C (2004) Sexual discrimination with cuticular lipids in Schoetella ununguiculata (Tullberg, 1869) (Collembola: Hypogastruridae). Pedobiologia 48:581–583Google Scholar
  118. Porco D, Deharveng L, Skarżyński D (2009) Sex pheromone in Tetrodontophora bielanensis (Waga, 1842) (Collembola: Onychiuridae): indirect reproduction mediated by cuticular compounds. Pedobiologia 53:59–63Google Scholar
  119. 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 213:66–82Google Scholar
  120. Puga-Freitas R, Blouin M (2015) A review of the effects of soil organisms on plant hormone signalling pathways. Environ Exp Bot 114:104–116Google Scholar
  121. Purrington FF, Kendall PA, Bater JE, Stinner BR (1991) Alarm pheromone in a gregarious poduromorph collembolan (Collembola: Hypogastruridae). Great Lakes Entomol 24:75–78Google Scholar
  122. Reddy GVP, Guerrero A (2004) Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci 9:253–261Google Scholar
  123. 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 565:8–27Google Scholar
  124. Roelofs WL, Brown RL (1982) Pheromones and evolutionary relationships of Tortricidae. Annu Rev Ecol Syst 13:395–422Google Scholar
  125. Rollo CD, Czyzewska E, Borden JH (1994) Fatty acid necromones for cockroaches. Naturwissenschaften 81:409–410Google Scholar
  126. Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. mBio 7:e01395–e01315Google Scholar
  127. Rosenstiel TN, Shortlidge EE, Melnychenko AN, Pankow JF, Eppley SM (2012) Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss. Nature 489:431–433Google Scholar
  128. 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 34:179–188Google Scholar
  129. Salmon S (2001) Earthworm excreta (mucus and urine) affect the distribution of springtails in forest soils. Biol Fertil Soils 34:304–310Google Scholar
  130. Salmon S (2004) The impact of earthworms on the abundance of Collembola: improvement of food resources or of habitat? Biol Fertil Soils 40:323–333Google Scholar
  131. Salmon S, Ponge JF (1999) Distribution of Heteromurus nitidus (Hexapoda, Collembola) according to soil acidity: interactions with earthworms and predator pressure. Soil Biol Biochem 31:1161–1170Google Scholar
  132. Salmon S, Ponge JF (2001) Earthworm excreta attract soil springtails: laboratory experiments on Heteromurus nitidus (Collembola: Entomobryidae). Soil Biol Biochem 33:1959–1969Google Scholar
  133. Salmon S, Geoffroy JJ, Ponge JF (2005) Earthworms and Collembola relationships: effects of predatory centipedes and humus forms. Soil Biol Biochem 37:487–495Google Scholar
  134. Sánchez-García A, Peñalver E, Delclòs X, Engel MS (2018) Mating and aggregative behaviors among basal hexapods in the Early Cretaceous. PLoS One 13:e0191669Google Scholar
  135. Sanon A, Andrianjaka ZN, Prin Y, Bally R, Thioulouse J, Comte G, Duponnois R (2009) Rhizosphere microbiota interferes with plant-plant interactions. Plant Soil 321:259–278Google Scholar
  136. Sbarbati A, Osculati F (2006) Allelochemical communication in vertebrates: kairomones, allomones and synomones. Cells Tissues Organs 183:206–219Google Scholar
  137. Schooley RL, Wiens JA (2003) Finding habitat patches and directional connectivity. Oikos 102:559–570Google Scholar
  138. Seastedt TR (1984) The role of microarthropods in decomposition and mineralization process. Annu Rev Entomol 29:25–46Google Scholar
  139. 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 110:4853–4853Google Scholar
  140. Shorey HH (1973) Behavioural responses to insect pheromones. Annu Rev Entomol 18:349–380Google Scholar
  141. 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 188:734–736Google Scholar
  142. 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 43:1411–1416Google Scholar
  143. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. BioScience 51:235–246Google Scholar
  144. Stam E, Isaaks A, Ernsting G (2002) Distant lovers: spermatophore deposition and destruction behaviour by male springtails. J Insect Behav 15:253–268Google Scholar
  145. Stamps JA, Swaisgood RR (2007) Someplace like home: experience, habitat selection and conservation biology. Appl Anim Behav Sci 102:392–409Google Scholar
  146. Stökl J, Steiger S (2017) Evolutionary origin of insect pheromones. Curr Opinion Insect Sci 24:36–42Google Scholar
  147. Stötefeld L, Scheu S, Rohlfs M (2012) Fungal chemical defence alters density-dependent foraging behaviour and success in a fungivorous soil arthropod. Ecol Entomol 37:323–329Google Scholar
  148. Symonds MRE, Elgar MA (2004) The mode of pheromone evolution: evidence from bark beetles. Proc R Soc Lond B 271:839–846Google Scholar
  149. Symonds MRE, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228Google Scholar
  150. Symonds MRE, Wertheim B (2005) The mode of evolution of aggregation pheromones in Drosophila species. J Evol Biol 18:1253–1263Google Scholar
  151. Taga ME, Bassler BL (2003) Chemical communication among bacteria. Proc Natl Acad Sci U S A 100:14549–14554Google Scholar
  152. Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ (1999) Insect pheromones: an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol 29:481–514Google Scholar
  153. Usher MB (1969) Some properties of the aggregations of soil arthropods: Collembola. J Anim Ecol 38:607–622Google Scholar
  154. Usher MB, Balogun RA (1966) A defence mechanism in Onychiurus (Collembola, Onychiuridae). Entomol Monthly Mag 102:237–238Google Scholar
  155. Van Arnam EB, Currie CR, Clardy J (2018) Defense contracts: molecular protection in insect-microbe symbioses. Chem Soc Rev 47:1638–1651Google Scholar
  156. Veen GF, Freschet GT, Ordonez A, Wardle DA (2015) Litter quality and environmental controls of home-field advantage effects on litter decomposition. Oikos 124:187–195Google Scholar
  157. Verhoef HA (1984) Releaser and primer pheromones in Collembola. J Insect Physiol 30:665–670Google Scholar
  158. Verhoef HA, Nagelkerke CJ (1977) Formation and ecological significance of aggregations of Collembola. Oecologia 31:215–226Google Scholar
  159. Verhoef HA, Nagelkerke CJ, Joosse ENG (1977a) Aggregation pheromones in Collembola. J Insect Physiol 23:1009–1013Google Scholar
  160. Verhoef HA, Nagelkerke CJ, Joosse ENG (1977b) Aggregation pheromones in Collembola (Apterygota): a biotic cause of aggregation. Rev Écol Biol Sol 14:21–25Google Scholar
  161. Vet LEM (1999) From chemical to population ecology: infochemical use in an evolutionary context. J Chem Ecol 25:31–49Google Scholar
  162. Waldorf ES (1974a) Sex pheromone in the springtail, Sinella curviseta. Environ Entomol 3:916–918Google Scholar
  163. Waldorf ES (1974b) Variations in cleaning between the sexes of Sinella coeca (Collembola: Entomobryidae). Psyche 81:254–257Google Scholar
  164. Waldorf ES (1976) Antennal amputation in Sinella curviseta (Collembola: Entomobryidae). Ann Entomol Soc Am 69:841–842Google Scholar
  165. Wall DH, Moore JC (1999) Interactions underground: soil biodiversity, mutualism, and ecosystem processes. BioScience 49:109–117Google Scholar
  166. 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 29:155–160Google Scholar
  167. Wehner K, Norton RA, Blüthgen N, Heethoff M (2016) Specialization of Oribatid mites to forest microhabitats: the enigmatic role of litter. Ecosphere 7:e01336Google Scholar
  168. Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506Google Scholar
  169. Wertheim B, Van Baalen EJA, Dicke M, Vet LEM (2005) Pheromone-mediated aggregation in non-social arthropods: an evolutionary ecological perspective. Annu Rev Entomol 50:321–346Google Scholar
  170. Westerberg L, Lindström T, Nilsson E, Wennergren U (2008) The effect on dispersal from complex correlations in small-scale movement. Ecol Model 213:263–272Google Scholar
  171. 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 103:52–62Google Scholar
  172. Wilson EO, Bossert WH (1963) Chemical communication among animals. Recent Prog Horm Res 19:673–716Google Scholar
  173. 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 88:15–30Google Scholar
  174. Zhao C, Griffin JN, Wu XW, Sun SC (2013) Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. J Anim Ecol 82:749–758Google Scholar
  175. 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 78:1261–1267Google Scholar
  176. 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 124:221–227Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Sandrine Salmon
    • 1
  • Sylvie Rebuffat
    • 2
  • Soizic Prado
    • 2
  • Michel Sablier
    • 3
  • Cyrille D’Haese
    • 1
  • Jian-Sheng Sun
    • 4
  • Jean-François Ponge
    • 1
    Email author
  1. 1.Département Adaptations du Vivant, UMR 7179 MECADEVMuséum National d’Histoire NaturelleParisFrance
  2. 2.Département Adaptations du Vivant, UMR 7245 MCAMMuséum National d’Histoire NaturelleParisFrance
  3. 3.Département Origines et ÉvolutionMuséum National d’Histoire NaturelleParisFrance
  4. 4.Département Adaptations du VivantMuséum National d’Histoire NaturelleParisFrance

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