Abstract
Stressful environmental conditions generally limit animal survival, growth, and reproduction and may induce dormancy in the form of various resting stages. Tardigrades represent one of a few animal phyla in which different forms of dormancy are frequently encountered. One of these forms, cryptobiosis, a quick response to sudden changes in the environment, has gained a great deal of attention, whereas much less is known of the slower emerging form of dormancy, diapause. In this review we present the current knowledge of diapause in tardigrades.
Diapause in tardigrades, represented by encystement and cyclomorphosis, is likely controlled by exogenous stimuli, such as temperature and oxygen tension, and perhaps also by endogenous stimuli. These stimuli initiate and direct successive phases of deep morphological transformations within the individual. Encystment is characterized by tardigrades that lie dormant—in diapause—within retained cuticular coats (exuvia). The ability to form cysts is likely widespread but presently only confirmed for a limited number of species.
In tardigrades, cyclomorphosis was first reported as a characteristic of the marine eutardigrade genus Halobiotus. This phenomenon is characterized by pronounced seasonal morphological changes and in Halobiotus involves stages with an extra protecting cuticle. Cyst formation in moss-dwelling limnic species may also occur as part of a seasonal cyclic event and can thus be viewed as part of a cyclomorphosis. Therefore, whereas diapause generally seems to be an optional response to environmental changes, it may also be an obligate part of the life cycle.
The evolution of encystment and cyclomorphosis finds its starting point in the molting process. Both phenomena represent an adaptation to environmental constraints. Notably, the evolution of diapause is not necessarily an alternative to cryptobiosis, and some tardigrades may enter both forms of dormancy. The simultaneous occurrence of several adaptive strategies within tardigrades has largely increased the resistance of these enigmatic animals toward extreme environmental stress.
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References
Bertolani R (1976) Osservazioni cariologiche su Isohypsibius augusti (Murray, 1907) e I. megalonyx Thulin, 1928 (Tardigrada) e ridescrizione delle due specie. Boll Zool 43:221–234
Bertolani R (1982) 15. Tardigradi (Tardigrada). Guide per il riconoscimento delle specie animali delle acque interne Italiane. Consiglio Nazionale Delle Ricerche, Verona, Italy, p 104
Biserov VI (1992) A new genus and three new species of tardigrades (Tardigrada: Eutardigrada) from the USSR. Boll Zool 59:95–103
Càceres CE (1997) Dormancy in invertebrates. Invertebr Biol 116:371–383
Clausen LKB, Andersen KN, Hygum TL, Jørgensen A, Møbjerg N (2014) First record of cysts in the tidal tardigrade Echiniscoides sigismundi. Helgol Mar Res 68(4):531–537. https://doi.org/10.1007/s10152-014-0409-0
Crowe JH, Newell IM, Thomson WW (1971) Cuticle formation in the tardigrade, Macrobiotus areolatus Murray. J Microsc 11:121–132
Denlinger DL, Tanaka S (1999) Diapause. In: Knobil E, Neill JD (eds) Encyclopedia of Reproduction, vol 1. Academic Press, San Diego, pp 863–872
Diaz Cosin DJ, Riuz MP, Ramajo M, Gutiérrez M (2006) Is the aestivation of the earthworm Hormogaster elisae a paradiapause? Invertebr Biol 125:250–255
Doyère M (1840) Mémoiresur les Tardigrades. Ann Sci Naturelles, Paris, Ser 2, Zool 14:269–361
Eibye-Jacobsen J (1997) Development, ultrastructure and function of the pharynx of Halobiotus crispae Kristensen, 1982 (Eutardigrada). Acta Zool 78:329–347
Eibye-Jacobsen J (2001) Are the supportive structures of the tardigrade pharynx homologous throughout the entire group? J Zool Syst Evol Research 39:1–11
Guidetti R, Boschini D, Rebecchi L, Bertolani R (2006) Encystment processes and “Matrioshka-like stage” cyst in a moss-dwelling and in a limnic species of eutardigrades (Tardigrada). Hydrobiologia 558:9–21
Guidetti R, Boschini D, Altiero T, Bertolani R, Rebecchi L (2008) Diapause in tardigrades: a study of factors involved in encystment. J Exp Biol 211:2296–2302
Gullan PJ, Cranston PS (2005) The Insects: an outline of entomology, 3rd edn. Blackwell, Oxford, p 505
Guidetti R, Altiero T, Rebecchi L (2011) On dormancy strategies in tardigrades. J Insect Physiol 57(5):567–576
Halberg KA, Persson D, Ramløv H, Westh P, Kristensen RM, Møbjerg N (2009) Cyclomorphosis in Tardigrada: adaptation to environmental constraints. J Exp Biol 212(17):2803–2811
Halberg KA, Persson DK, Jørgensen A, Kristensen RM, Møbjerg N (2013a) Ecology and thermal tolerance of the marine tardigrade Halobiotus crispae (Eutardigrada: Isohypsibiidae). Mar Biol Res 9(7):716–724
Halberg KA, Larsen KW, Jørgensen A, Ramløv H, Møbjerg N (2013b) Inorganic ion composition in Tardigrada: cryptobionts contain large fraction of unidentified organic solutes. J Exp Biol 216:1235–1243
Hansen JG, Katholm AK (2002) A study of the genus Amphibolus from Disko Island with special attention on the life cycle of Amphibolus nebulosus (Eutardigrada: Eohypsibiidae). In: Hansen JG (ed) Arctic Biology Field Course Quqertarsuaq 2002. Zoological Museum University of Copenhagen, Copenhagen, pp 129–163
Heinis F (1910) Systematik und Biologie der Moosebewohnen den Rhizopoden, Rotatorien und Tardigraden usw. Archiv für Hydrobiologie und Plankton kund: 51–115
Hygum TL, Fobian D, Kamilari M, Jørgensen A, Schiøtt M, Grosell M, Møbjerg N (2017) Comparative investigation of copper tolerance and identification of putative tolerance related genes in tardigrades. Front Physiol 8:95. https://doi.org/10.3389/fphys.2017.00095
Iharos G (1968) The scientific results of the Hungarian soil zoological expeditions to South America: 6. Ein neue Tardigraden-Gattung von mariner Verwandtschaft aus dem chilenischen Altiplano. Opusc Zool 7:357–361
Koštál V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127
Kristensen RM (1982) The first record of cyclomorphosis in Tardigrada based on a new genus and species from Arctic meiobenthos. J Zool Syst Evol 20:249–270
Kristensen RM (1987) Generic revision of the Echiniscidae (Heterotardigrada) with a discussion of the origin of the family. In: Biology of tardigrades, pp 261–335
Lauterborn R (1906) Demostrationen aus der Fauna ders Oberreheins und seiner Umgebung. Verh Dtsch Zool Ges:265–268
Manicardi GC (1989) Two new species of soil moss eutardigrades (Tardigrada) from Canada. Can J Zool 67(9):2282–2285
Marcus E (1929) Tardigrada. In: Bronns HG (ed) Klassen und Ordnungen des Tierreichs, vol 5. Akademische Verlagsgesellschaft, Leipzig, Germany, p 608
Marcus E (1936) Tardigrada. In: Schulze FE, Kükenthal W, Heider K (eds) Das Tierreich, vol 66. Walter de Gruyter Berlin und Leipzig, Germany, pp 1–340
Marley NJ, Wright DE (1996) Amphibolus weglarskae (Dastych), a new addition to the Tardigrada of Iceland with an updated checklist of Icelandic species (Eohypsibiidae, Eutardigrada). Quekett J Microsc 37:541–545
Maucci W (1987) A contribution to the knowledge of the North American Tardigrada with emphasis on the fauna of Yellowstone National Park (Wyoming). In: Biology of Tardigrades. Selected Symposia and Monographs UZI, vol 1, pp 187–210
McInnes SJ, Pugh PJA (1999) Zonation in Antarctic lake-dwelling benthic meiofauna, with emphasis on the Tardigrada. Zool Anz 238:283–288
Møbjerg N, Jørgensen A, Eibye-Jacobsen J, Halberg KA, Persson D, Kristensen RM (2007) New records on cyclomorphosis in the marine eutardigrade Halobiotus crispae (Eutardigrada: Hypsibiidae). J Limnol 66(Suppl 1):132–140
Møbjerg N, Halberg KA, Jørgensen A, Persson D, Bjørn M, Ramløv H, Kristensen RM (2011) Survival in extreme environments – on the current knowledge of adaptations in tardigrades. Acta Physiol 202(3):409–420
Murray J (1907a) The encystment of Macrobiotus. Fortschr Zool 11:4–11
Murray J (1907b) Encystment of Tardigrada. Trans R Soc Edinb 45:837–854
Murray J (1907c) Some Tardigrada of the Sikkim Himalaya. J R Microsc Soc 3:269–273
Murray J (1907d) XXIV – Scottish Tardigrada, collected by the Lake Survey. Trans R Soc Edinb 45:641–668
Nederström P (1919) Die bisjetzt aus Finnland bekannten Tardigraden. Act Soc Fraun Flor Fenn 46(8):1–15
Pigòn A, Węglarska B (1953) The respiration of Tardigrada: a study in animal anabiosis. Bull Acad Pol Sci Biol 1:69–72
Rahm G (1925) Die Cysten bildung bei den WasserbewohnendenTardigraden. Int Ver Theor Angew Limnol Verh 3:364–371
Rahm G (1926) Die Trockenstarre (Anabiose) der Moostierwelt. Biol Cent Bl 46:452–477
Rahm G (1927) Tardigrada Biolog d Tiere Deutschland 22:1–56
Ramazzotti G (1959) Tardigradi in terreni prativi. Atti Soc Ital Nat, Milano 98:199–210
Ramazzotti G, Maucci W (1983) Il Phylum Tardigrada. Terza edizione riveduta e corretta. Mem Isit Ital Idrobiol Dott Marco De Marchi 41:1–1012
Rebecchi L, Bertolani R (1994) Maturative pattern of ovary and testis in eutardigrades of freshwater and terrestrial habitats. Invertebr Reprod Dev 26:107–117
Richters F (1909) Tardigraden-Studien. Ber Senckenb Naturforsch Ges 40:28–45
Richters F, Krumbach T (1926) Tardigrada. Handbuch der Zoologie 3:1–68
Rost-Roszkowska M, Poprawa I (2008) Ultrastructure of the midgut epithelium in Dactylobiotus dispar (Tardigrada: Eutardigrada) during encystation. Zool Polon 53(1-4):19–25
Schill RO, Huhn F, Köhler HR (2007) The first record of tardigrades (Tardigrada) from the Sinai Peninsula, Egypt. Zool Middle East 42(1):83–88
Schultze M (1865) Echiniscus sigismundi, ein Arctiscoide der Nordsee. Arch Mikrosk Anat 1(1):428–436
Sommerville RI, Davey KG (2002) Diapause in parasitic nematodes: a review. Can J Zool 80:1817–1840
Stark S, Kristensen RM (1999) Tardigrades in the soil of Greenland. Ber Polarforsch 330:44–63
Szymańska B (1995) Encystment in the tardigrade Dactylobiotus dispar (Murray, 1907) (Tardigrada: Eutardigrada). Part 1: Observation of leaving animals and structure of cyst. Zool Pol 40:91–102
Thulin G (1911) Beiträge zur Kenntnis der Tardigraden fauna Schwedens. Ark Zool 7(16):1–60
Thulin G (1928) Über die Phylogenie und das System der Tardigraden. Hereditas 11:207–266
Urbanowicz C (1925) Sur la variabilité de Macrobiotus oberhaeuseri. Bull biol Fr Bel 59:124–142
Von Reukauf EW (1912) Ein neuer Wasserbär, Macrobiotus ferdinandi (Reukauf). Zool Anz 39:352–353
von Wenck V (1914) Entwicklungs geschichtliche Untersuchungen an Tardigraden (Macrobiotus lacustris Duj.). Zool Jahrb Anat 37:465–514
Węglarska B (1957) On the encystation in Tardigrada. Zool Pol 8:315–325
Węglarska B (1970) Hypsibius (Isohypsibius) smreczynskii spec. nov., a new species of fresh-water tardigrade. Zesz Nauk Uniw Jagiellonsk Pr Zool 16:107–114
Wełnicz W, Grohme MA, Kaczmarek L, Schill R, Frohme M (2011) Anhydrobiosis in tardigrades – the last decade. J Insect Physiol 57:577–583
Westh P, Kristensen RM (1992) Ice formation in the freeze-tolerant eutardigrades Adorybiotus coronifer and Amphibolos nebulosus studied by differential scanning calorimetry. Polar Biol 12:693–699
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Guidetti, R., Møbjerg, N. (2018). Environmental Adaptations: Encystment and Cyclomorphosis. In: Schill, R. (eds) Water Bears: The Biology of Tardigrades. Zoological Monographs, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-319-95702-9_9
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