Advertisement

Introduction to Dormancy in Aquatic Invertebrates: Mechanism of Induction and Termination, Hormonal and Molecular-Genetic Basis

  • Victor R. AlekseevEmail author
  • Elena B. Vinogradova
Chapter
Part of the Monographiae Biologicae book series (MOBI, volume 92)

Abstract

Dormancy is a profound and ancient adaptation found in a wide spectrum of plants and animals of all habitats. In diapause, the switch between active and dormant states is driven by hormonal mechanism that usually includes a photoperiodic pacemaker. Temperature, food limitation, and some other stress factors as well are shown as driven by diapause induction in aquatic invertebrates. In the last decade, diapause studies from a wide variety of topics have demonstrated that diapause switch mechanisms may be developed to create novel applications in biotechnology. Resting eggs accumulated in the surface lake sediments represent a “bank” of zooplankton species that assures their persistence in a community, in spite of periodic harsh conditions.

Studies on the vertical distribution of resting eggs in sediment cores yield useful information to opening important perspectives for paleolimnological climate reconstruction and paleoecology. Cultivation of live food, like rotifers, Daphnia, Artemia, or marine copepods, is an expanding application of practical use of diapause in modern aquaculture. Biotechnologies can now be imagined for maintaining ecosystems outside the Earth’s biosphere. Resting stages provide at least two properties highly suitable for such ecosystems. They can be easily transported in space for a long time without special care as compared with an active ecosystem. In addition, storage of seeds and diapausing animals will provide a reserve in case of an unpredictable destruction of the active part of an ecosystem caused, for example, by a meteorite strike.

The term alien species takes on a new meaning when one considers another aspect of space biology. By enlarging the distribution area of the species, colonization of new environments could be a safeguard against its extinction. Thus, it would also be important to develop technologies to guard against invasions of other species via ship ballast waters and similar means.

We also suggest that molecular-genetic insights of diapause in invertebrates provide new ways of looking at carcinogenesis. Tumor cells may have parallels in postdiapause embryonic cells.

Keywords

Dormancy Signal factors Diapause in invertebrates Environmental factors Photoperiod Terminology 

References

  1. Aiken DE (1969) Photoperiod, endocrinology and the crustacean molt cycle. Science 164:149–155CrossRefGoogle Scholar
  2. Aiken DE (1981) Molting and growth. In: The biology and management of the Lobster, vol 1. Academic, New York, pp 136–163Google Scholar
  3. Aiken DE, Waddy SL (1981) Reproductive biology. In: The biology and management of the Lobster, vol 1. Academic, New York, pp 215–276Google Scholar
  4. Alekseev VR (1984) Effect of chlorine treatment on zooplankton in sturgeon nursery fish ponds. Trans State Lakes Rivers Res Inst 225:95–104. in RussianGoogle Scholar
  5. Alekseev VR (1986) Role of diapause in acclimatization of crustaceans. Proc GosNIORKH 252:61–68. in RussianGoogle Scholar
  6. Alekseev VR (1989) Effect of diapause on oxygen consumption in. Astacidae Tr GosNIORKh 300:80–90Google Scholar
  7. Alekseev VR (1990) Diapauza rakoobraznykh: ekologo-fiziologicheskie aspekty (Diapause in Crustacea: ecological–physiological aspects). Nauka, Moscow, 144 pp (in Russian)Google Scholar
  8. Alekseev VR (1998) Biochemical and physiological characteristics of Crustaceans in diapause: the internal mechanism of reactivation. Arch Hydrobiol 52:463–476Google Scholar
  9. Alekseev VR (2004) Effects of dial vertical migration on ephippia production in Daphnia. J Limnol 63:1–6CrossRefGoogle Scholar
  10. Alekseev V, Lampert W (2001) Maternal control of resting egg production in Daphnia. Nature 414:899–901CrossRefGoogle Scholar
  11. Alekseev V, Lampert W (2004) Maternal effects of photoperiod and food level on life history characteristics of the cladoceran Daphnia pulicaria Forbes. Hydrobiologia 526:225–230CrossRefGoogle Scholar
  12. Alekseev VR, Starobogatov YI (1996) Types of diapause in Crustacea: definitions, distributions, evolution. Hydrobiologia 320:15–26CrossRefGoogle Scholar
  13. Alekseev VR, Sychev VN (2006) Effect of space station conditions on resting egg survivorship and parameters of life cycle in D. magna. Abst COSPAR Beijin July 2006Google Scholar
  14. Alekseev VR, Pinel-Alloul B, Methot J (1999) Role of summer cyclopid diapause in lake meyobenthos forming in Quebec lakes (Canada). Abst. Annual scientific session of Zoological Institute, Academic Publishers, St. Petersburg 8–9 (in Russian)Google Scholar
  15. Alekseev VR, Djenderedjan K, Fiks B (2001) Role of summer diapause in success of invasion of a new invertebrate predator into plankton ecosystem of a large mountain lake. In: Proceedings of 9th International Conference conservation and management of lakes, BIWAKO, Japan, pp 41–47Google Scholar
  16. Alekseev V, Dumont H, Pensaert J, Baribwegure D, Vanfleteren JR (2006a) A redescription of Eucyclops serrulatus (Fischer, 1851) (Crustaceaa, Copepoda, Cyclopoida) and some related taxa, with a phylogeny of the E. serrulatus-group. Zooogica Scripta 35:123–158CrossRefGoogle Scholar
  17. Alekseev VR, Sychev VN, Novikova NI (2006b) Studying the phenomenon of dormancy: why it is important for space exploration. Abst. COSPAR Beijin July 2006Google Scholar
  18. Alekseev VR, de Stasio BT, Gilbert JJ (eds) (2007) Diapause in aquatic invertebrates: theory and human use. Monographiae Biologicae 84. Springer, Dordrecht, 257 p.Google Scholar
  19. Antebi A, Yeh WH, Tait D, Hedgecock EM, Riddle DL (2000) daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 14:1512–1527PubMedPubMedCentralGoogle Scholar
  20. Apfeld J, Kenyon C (1989) Cell Nonautonomy of C. elegans daf 2 function in the regulation of diapause and lifespan. Cell 95:199–210CrossRefGoogle Scholar
  21. Arbaciauskas K (1998) Life history traits of Exephippial and par thenogenetically derived Daphnids: indicators of different life history strategies. Adv Limnol 52:339–358Google Scholar
  22. Arbačiauskas K (2001) Life-history variation related to the first adult instar in daphnids derived from diapausing and subitaneous eggs. Hydrobiologia 442:157–164CrossRefGoogle Scholar
  23. Arbačiauskas K (2004) Seasonal phenotypes of Daphnia: post-diapause and directly developing offspring. J Limnol 63:7–15CrossRefGoogle Scholar
  24. Askerov MK, Sidorov PA (1964) Biology of phyllopods in sturgeon ponds and struggle against the crustaceans. Trans Azerbajdjan Res Inst Fish Ind 4:83–97. in RussianGoogle Scholar
  25. Baldwin WS, LeBlanc GA (1994) Identification of multiple steroid hydroxylases in Daphnia magna and their modulation by xenobiotics. Environ Toxicol Chem 13:1013–1021CrossRefGoogle Scholar
  26. Banta AM, Brawn LA (1929) Control of sex in Сladocera. 1. Crowding the mothers as a means of controlling male production. Physiol Zool 2:80–92CrossRefGoogle Scholar
  27. Behning AL (1941) Cladocera of the Caucuses, Gruzmedizdat Tbilisi (in Russian)Google Scholar
  28. Berg K (1934) Cyclic reproduction, sex determination and depression in Cladocera. Camb Biol Rev 9:1CrossRefGoogle Scholar
  29. Bliss DE (1966) Relation between reproduction and growth in decapod Crustaceans. Am Zool 6:231–233PubMedCrossRefGoogle Scholar
  30. Bogatova IB, Erofeeva GI (1985) Incubation of Artemia salina resting eggs without preliminary stimulation. Hydrobiol J 21:52–56 (in Russian)Google Scholar
  31. Bouchon D, Remoissenent G, Mocquard JP (1985) Influence de la temperature sur 1’entree en reproduction de Palaemonetes varians Leach (Crustace, Decapoda, Natantia). Bull Sci Zool Fr 110:439–447Google Scholar
  32. Bradshaw WE, Holzapfel CM (2001) Genetic shift in photoperiodic response correlated with global warming. Proc Natl Acad Sci USA 98:14509–14511PubMedCrossRefGoogle Scholar
  33. Branford GK (1978) The influence of day-length, temperature and season on the hatching rhythm of Homarus gammarus. J Mar Biol Assoc UK 58:639–658CrossRefGoogle Scholar
  34. Bunning E (1936) Die Endonom Tagesrhythmik Als Grundlage der Photoperiodischen Reakton. Ber Deut Bot Ges 54:590–607Google Scholar
  35. Burner HC, Halcrow K (1977) Experimental induction of the production of ephippia by Daphnia magna Straus (Cladocera). Crustaceana 32:77–86CrossRefGoogle Scholar
  36. Cáceres CE (1997) Temporal variation, dormancy, and coexistence: a field test of the storage effect. Proc Natl Acad Sci USA 94:9171–9175PubMedCrossRefGoogle Scholar
  37. Carlisle DB (1957) On the hormonal inhibition of moulting in decapod Crustacea. J Mar Biol Ass UK 36:291–307CrossRefGoogle Scholar
  38. Carlisle DB, Pitman WJ (1961) Diapause, neurosecretion and hormones in Copepoda. Nature 190:827–828PubMedCrossRefGoogle Scholar
  39. Carvalho GR, Wolf HG (1989) Resting eggs of lake-Daphnia I. Distribution, abundance and hatching of eggs collected from various depths in lake sediments. Freshw Biol 22:459–470CrossRefGoogle Scholar
  40. Cassada R, Russell R (1975) The Dauer Larva: a post embryonic developmental variant of the Nematode C. elegans. Dev Biol 46:326–342PubMedCrossRefGoogle Scholar
  41. Champeau A (1970) Etude de la vie latente chez des Calanoides (Copepodes) caracteristiques des eaux temperairres de Basse—Provence. Ann Fac Sci Marseille 44:155–189Google Scholar
  42. Chang ES (1984) In: Engels W et al (eds) Ecdysteroids in Crustacea: role in reproduction, molting, and larval development advances in invertebrate reproduction, vol 3. Elsevier, Amsterdam, pp 223–249Google Scholar
  43. Coker RE (1933) Arret du developpement chez les copepodes. Bull Biol 67:276–287Google Scholar
  44. Cooley JM (1971) The effect of temperature on the development of resting eggs of Diaptomus oregonensis Lillj (Copepoda:Calanoida). Limnol Oceanogr 16:921–926CrossRefGoogle Scholar
  45. Crag TL, Denlinger DL (2000) Sequence and transcription patterns of 60S ribosomal protein P0 a diapause regulated AP endonuclease in the flesh fly, Sarcophaga crassipalpis. Gene 255:381–388CrossRefGoogle Scholar
  46. Crisp DJ, Patel B (1969) Environmental control of the breeding of three boreoarctic cirripedes. Mar Biol 2:283–295CrossRefGoogle Scholar
  47. da Graca LS, Zimmerman KK, Mitchell MC, Kozhan-Gorodetska M, Sekiewicz K, Morales Y, Patterson GI (2003) DAF-5 is a Ski oncoprotein homolog that functions in a neuronal TGFb pathway to regulate C. elegans dauer development. Development 131:435–446PubMedCrossRefPubMedCentralGoogle Scholar
  48. Danilevsky AS (1961) Fotoperiodizm i sezonnoe razvitie nasekomykh (Photoperiodism and seasonal development of insects). Lening Gos University, Leningrad, 243 pp (In Russian)Google Scholar
  49. De Stasio BT Jr (1990) The role of dormancy and emergence patterns in the dynamics of a freshwater zooplankton community. Limnol Oceanogr 35:1079–1090CrossRefGoogle Scholar
  50. Demensy N (1958) Recherches sur la Mue de Pubert du Decapoda Brachyoure carcinus Maeneas. Arch Zool Exp Gen 95:253 pp.Google Scholar
  51. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122PubMedCrossRefGoogle Scholar
  52. Denlinger DL, Armbruster PA (2014) Mosquito diapause. Annu Rev Entomol 59:73–93.  https://doi.org/10.1146/annurev-ento-011613-162023CrossRefPubMedGoogle Scholar
  53. Denlinger DL, Yocum GD, Rinehart JP (2012) Hormonal control of diapause. In: Gilbert LI (ed) Insect endocrinology. Academic, San Diego, pp 430–463CrossRefGoogle Scholar
  54. Einsle U (1967) Die ausseren Bedingungen der Diapause plankisch lebender Cyclops-Arten. Arch Hydrobiol 63:387–403Google Scholar
  55. Finch CE, Ruvkun G (2001) The genetics of aging. Ann Rev Genom Hum Genet 2:435–462CrossRefGoogle Scholar
  56. Fries G (1964) Uber die Einwirkung der Tagesperiodik und der Temperatur auf den Generationswechsel, die Weibchengrosse und die Eir von Daphnia magna Straus. Ztschr Morphol und Okol Tierr 53:475–516CrossRefGoogle Scholar
  57. Fryer G (1996) Diapause a potent force in the evolution of freshwater crustaceans. Hydrobiologia 320:1–14CrossRefGoogle Scholar
  58. Fryer G, Smyly WIP (1954) Some remarks on the resting stagees of some fresh water cyclopoid and harpacticoid copepods. Ann Mag Nat Hist 7:65–72CrossRefGoogle Scholar
  59. Georgi LL, Albert PS, Riddle DL (1990) daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell 61:635–645PubMedCrossRefGoogle Scholar
  60. Gerisch B, Antebi A (2004) Hormonal signals produced by daf 9/cytochrome P450 regulate C. elegans Dauer Dia pause in response to environmental cues. Development 131:1765–1776CrossRefGoogle Scholar
  61. Gerisch B, Weitzel C, Kober-Eisermann C, Rottiers V, Antebi A (2001) A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and lifespan. Dev Cell 1:841–851PubMedCrossRefPubMedCentralGoogle Scholar
  62. Gilbert JJ, Thompson GA Jr (1968) Alpha tocopherol control of sexuality and polymorphism in the rotifer Asplanchna. Science 159:734–736PubMedCrossRefPubMedCentralGoogle Scholar
  63. Gliwicz ZM, Rowan MG (1984) Survival of Cyclops Abyssorum tatricus (Copepoda, Crustacea) in Alpine Lakes stocked with Planktivrous fish. Limnol Oceanogr 29:1290–1299CrossRefGoogle Scholar
  64. Golden JW, Riddle DL (1984) The Caenorhabditis elegans Dauer Larva: developmental effects of pheromone, food, and temperature. Dev Biol 102:368–378PubMedCrossRefPubMedCentralGoogle Scholar
  65. Grosvener G, Smith G (1913) The life cycle of Moina rectirostris. Q J Microsc Soc 58:87–112Google Scholar
  66. Hairston NG Jr, Cáceres C (1996) Distribution of crustacean diapause: Micro- and macroevolutionary pattern and process. Hydrobiologia 320:27–44CrossRefGoogle Scholar
  67. Hairston NG Jr, Olds EJ (1987) Population differences in the timing of diapause: A test of hypotheses. Oecologia 71:339–344PubMedCrossRefGoogle Scholar
  68. Henderson ST, Johnson TE (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11:1975–1980PubMedCrossRefGoogle Scholar
  69. Herman AW, Sameoto DD, Longhurst AR (1981) Vertical and horizontal distribution patterns of copepods near the shelf .break front south of Nova Scotia, Canad. J Fish Aquatic Sci 38:1065–1076CrossRefGoogle Scholar
  70. Hirche HJ (1996) Diapause in the marine copepod, Calanus finmarchicus – a review. Ophelia 44:129–143CrossRefGoogle Scholar
  71. Ichikawa T (2003) Firing activities of neurosecretory cells producing diapause hormone and its related peptides in the female silkmoth, Bombyx mori. I. Labial cells. Zool Sci 20:971–978PubMedCrossRefGoogle Scholar
  72. Ivleva IV (1981) Temperature and metabolic rates in aquatic animals, Kiev. Naukova Dumka Publishers (in Russian)Google Scholar
  73. Iwami M (2000) Bombyxin: an insect brain peptide that belongs to the insulin family. Zool Sci 17:1035–1044PubMedCrossRefGoogle Scholar
  74. Jassem W, Mocquard JP, Juchault P (1982) Determinisme de la reproduction saisonniere des femelles d’Armadillidium vulgare Latr. (Crustace, Isopode, Oniscoide) IV. Contribution a la connaissance de la perception du signal photopreriodique in duisant 1’entree en reproduction: mode de discrimination entre Ie Jour et la mit longueurs d’onde actives. Ann Sci Nat Zool et Biol Anim 4:85–90Google Scholar
  75. Jia K, Albert PS, Riddle DL (2002) daf 9, a cytochrome P450 regulating C. elegans larval development and adult longevity. Development 129:221–231PubMedGoogle Scholar
  76. Johnson CL (2003) Ecdysteroids in the oceanic copepod Calanus pacificus: variation during molt cycle and change associated with diapause. Mar Ecol 257:159–165CrossRefGoogle Scholar
  77. Juchault P, Pavese A, Mocquard JP (1980) Determinisme de la reproduction saisonniere des femelles d’Armadillidium vulgare Latr. (Crustacea, Isopode, Oniscoide) II. Etude phiques differentes. Ann Sci Nat Zool et Biol Anim 2:99–108Google Scholar
  78. Kubersky ES (1977) Worldwide distribution and ecology of Alonopsis (Cladocera, Chydoridae) with a description of Alonopsis americana sp. nova, Intern Rev ges. Hydrobiology 62:649–685Google Scholar
  79. Lair KP, Bradshaw WE, Holzapfel CM (1997) Evolutionary divergence of the genetic architecture underlying photoperiodism in the pitcher-plant mosquito, Wyeomyia smithii. Genetics 147:1873–1883PubMedPubMedCentralGoogle Scholar
  80. Lampert W (2003) Evolutionary ecology: natural selection in freshwater systems. In: Moya A, Font E (eds) Evolution from molecules to ecosystems. University Press, Oxford, pp 109–121Google Scholar
  81. Laufer H, Ahl JSB, Sagi A (1993) The role of juvenile hormones in crustacean reproduction. Am Zool 33:365–374CrossRefGoogle Scholar
  82. Lee CL, Fieder DR (1982) Induced spawning in the freshwater prawn, Macrobrachium australiense Holthuis 1950 (Crustacea. Decapoda: Palaemonidae). Aquaculture 29:45–52CrossRefGoogle Scholar
  83. Lee RY, Hench J, Ruvkun G (2001) Regulation of C. elegans daf 16 and Its Human Ortholog FKHRL1 by the daf 2 Insulin Like Signaling Pathway. Curr Biol 11:1950–1957PubMedCrossRefGoogle Scholar
  84. Li W, Kennedy SG, Ruvku G (2003) daf 28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the daf 2 signaling pathway. Genes Dev 17:844–858PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lin K, Hsin H, Libina N, Kenyon C (2001) Regulation of the Caenorhabditis elegans longevity protein daf 16 by insulin/IGF 1 and germline signaling. Nat Genet (2):139–145PubMedCrossRefGoogle Scholar
  86. Little G (1968) Induced Winter Breeding and Larval Development in the Shrimp Palaemonetes pugio (Holthius), Crustaceana. Suppl 2:19–26Google Scholar
  87. MacRae TH (2005) Diapause: diverse states of developmental and metabolic arrest. J Biol Res 3:3–14Google Scholar
  88. Makrushin AV (1968) Condition of ephippial female ovary in some Cladocera species. Trans State Lakes Rivers Res Inst 67: 365–369 (in Russian)Google Scholar
  89. Makrushin AV, Stepanova IE (2003) Ob izberatenoj pronizaemosti obolochek latentnuh jaiz Moina macrocopa (Daphniiformes, Crustacea). (On the selective permeability of covering membrane in Moina macrocopa restin eggs). Zoologicheskij J 82:117–118Google Scholar
  90. Mansingh A (1971) Physiological classification of dormencies in insects. Can Entomol 103:983–1009CrossRefGoogle Scholar
  91. March BGE (1982) Decreased day length and light intensity as factors inducing reproduction in Gammarus lacustris Sars. Can J Zool 60:2962–2965CrossRefGoogle Scholar
  92. Marcus NH (1982) Photoperiodic and temperature regulation of diapause in Labidocera aestiva (Copepoda: Calanoida). Hydrobiologia 162:45–52Google Scholar
  93. Marcus NH (1986) Population dynamics of marine copepods: the importance of photoperiodism. Am Zool 26:469–477CrossRefGoogle Scholar
  94. Marcus NH (1996) Ecological and evolutionary significance of resting eggs in marine copepods: past, present and future studies. Hydrobiologia 320:141–152CrossRefGoogle Scholar
  95. Marcus NH, Lutz RV, Burnett W, Cable P (1994) Age, viability, and the vertical distribution of zooplankton resting eggs from an anoxic basin: evidence of an egg bank. Limnol Oceanogr 39:154–158CrossRefGoogle Scholar
  96. Mocquard JP, Juchault P (1985) Photoperiode et reproduction chez les femelles d’Armadillidium vulgare Latreille (Crustacea, Isopode, Oniscoide): variation en fonction de 1’origine geographique des populations. Bull Soc Zool Fr 110:425–439Google Scholar
  97. Monchenko VI (2003) Free living cyclopoid copepods of the Pontho-Caspian basin, Kiev. Naukova Dumka Academic Publishers (in Russian)Google Scholar
  98. Mori A, Romero-Severson J, Severson DW (2007) Genetic basis for reproductive diapauses is correlated with life history traits within Culex pipiens complex. Insect Mol Biol 16:515–524PubMedGoogle Scholar
  99. Morris JZ, Tissenbaum HA, Ruvkun G (1996) A phosphatidylinositol 3 OH Kinase family member regulating longevity and diapause in C. elegans. Nature 382:536–539PubMedCrossRefGoogle Scholar
  100. Mortimer CH (1936) Experimentelle und cytologische Untersuchungen liber den Generationswechsel der Cladoceren. Zool Jb Abt allg Zool und Physiol Tiere 56:323–388Google Scholar
  101. Munuswamy N, Nazar AK, Dumont HJ (1992) Is pH(i) a factor for dormancy in freshwater fairy shrimps. Curr Sci 62:751–752Google Scholar
  102. Naya Y, Mayumi O, Midori I, Wataru M (1989) What is molt inhibiting hormone? The role of an ecdysteroidogenesis inhibitor in the crustacean molting cycle. Proc Natl Acad Sci USA 86:6826–6829PubMedCrossRefGoogle Scholar
  103. Nelson RJ, Denlinger DL, Somers DE (eds) (2010) Photoperiodism: the biological calendar. Oxford University Press, New York, p 596Google Scholar
  104. Nilssen JP (1978) On the evolution of life histories of limnetic cyclopoid copepods. Memorie dell’Istituto Italiano di Idrobiologia 36:193–214Google Scholar
  105. Nilssen J, Elgmork K (1977) Cyclops abyssorum – life cycle dynamic and habitat selection. Memorie dell’Istituto Italiano di Idrobiologia 34:197–238Google Scholar
  106. Novak VJ (1966) Insect hormones. Methuen, London, 478 pp.Google Scholar
  107. Odum EP (1963) Ecology. New York/LondonGoogle Scholar
  108. Oehlmann J, Schulte Oehlmann U (2003) Endocrine disruption in invertebrates. Pure Appl Chem 75:2207–2218CrossRefGoogle Scholar
  109. Olmstead A, LeBlanc G (2000) Effects of endocrine active chemicals on the development of sex characteristics of Daphnia magna. Environ Toxicol Chem 19:2107–2113CrossRefGoogle Scholar
  110. Olmstead A, LeBlanc GA (2001) Temporal and quantitative changes in sexual reproductive cycling of the Cladoceran Daphnia magna by a juvenile hormone analog. J Exp Zool 290:148–155PubMedCrossRefGoogle Scholar
  111. Olmstead AW, LeBlanc GA (2003) Insecticidal juvenile hormone analogs stimulate the production of male offspring in the crustacean Daphnia magna. Environ Health Perspect 111:919–924PubMedPubMedCentralCrossRefGoogle Scholar
  112. Otsu T (1963) Bihonnonal control of the sexual cycle in the fresh water Crab Potamon dehaani. Embriologia 8:1–20CrossRefGoogle Scholar
  113. Owen RW (1981) Fronts and eddies in the sea: mechanism, interactions and biological effects. In: Longhurst AR (ed) Analysis of marine ecosystems. Academic Press, New YorkGoogle Scholar
  114. Pancella JR, Stross RG (1963) Light induced hatching of Daphnia resting eggs. Chesap Sci 4:404–425CrossRefGoogle Scholar
  115. Panov VE, Krylov PI, Riccardi N (2004) Role of diapause in dispersal and invasion success by aquatic invertebrates. J Limnol 63(Suppl 1):56–69CrossRefGoogle Scholar
  116. Parker R (1966) The influence of photoperiod on reproduction and molting of Daphnia schodleri Sars. Physiol Zool 39:266–279CrossRefGoogle Scholar
  117. Passano LM (1951) The X Organ, a neurosecretory gland controlling molting in crab. Anat Rec 1: 559 pp.Google Scholar
  118. Pierce SB, Costa M, Wisotzkey R, Devadhar S, Homburger SA, Buchman AR, Ferguson KC, Heller J, Platt DM, Pasquinelli AA (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev 15:672–686PubMedPubMedCentralCrossRefGoogle Scholar
  119. Pijanowska J (1997) Alarm signals in Daphnia. Oecologia 112:12–16PubMedCrossRefGoogle Scholar
  120. Poelchau MF, Reynolds JA, Elsik CG, Denlinger DL, Armbruster PA (2013) Deep sequencing reveals complex mechanism of diapauses preparation in the invasive mosquito, Aedes albopictus. Proc R Soc B 280:20130143PubMedCrossRefGoogle Scholar
  121. Pourriot R, Clement P (1973) Photoperiodisme et cycle heterogonique chez Notommata copeus (Rotifere, Monogonorte) II. In fluence de gualite de la lumiere Spectres d’action. Arch Zool Exp et Gen 114:277–300Google Scholar
  122. Qiu Z, MacRae TH (2007) Developmentally Regulated Synthesis of P8, a Stress Associated Transcription Cofactor, in Diapause Destined Embryos of Artemia franciscana. Cell Stress Chaperon 12:255–264CrossRefGoogle Scholar
  123. Quackenbush LS (1986) Crustacean endocrinology: a review. Can J Fish Aquat Sci 43:2271–2282CrossRefGoogle Scholar
  124. Robich RM, Denlinger DL (2005) Proc Natl Acad Sci USA 102:1512–1517CrossRefGoogle Scholar
  125. Sarojini R, Gyananth G (1985) Hormonal Control of Reproduction in the Freshwater prawn Macrobrachium lamerri. J Curr Biosci 2:111–116Google Scholar
  126. Sarvala J (1979) Bentic resting periods of pelagic cyclopods in an oligotrophic lake. Holarct Ecol 2:88–100Google Scholar
  127. Scharfenberg V (1914) Weitere Untersuchungen an Cladoceren liber die experimentel Lebeeinflussung des Geschlechts und der Dauereibildung. Intern Rev Ges Hydrobiol Biol Suppl 6:1–34CrossRefGoogle Scholar
  128. Shan RK (1974) Reproduction in laboratory stocks of Pleuroxus (Chydoridae, Cladocera) under influence of photoperiod and light intensity. Intern Rev Ges Hydrobiol 59:643–666CrossRefGoogle Scholar
  129. Shan RK, Frey DG (1968) Induced interbreeding between two stocks of a Chydorid Cladoceran. Bioscience 18:203–205CrossRefGoogle Scholar
  130. Shull AF (1943) Origin of diverse strains of an aphid species within a limited area. Pap Mich Acad Sci Arts Lett Pt II Zool 28:425–431Google Scholar
  131. Sim C, Denlinger DL (2008) Insulin signaling and FOXO regulate the overwintering diapauses of the mosquito Culex pipiens. Proc Natl Acad Sci USA 105:6777–6781PubMedCrossRefGoogle Scholar
  132. Skinner DM (1985) Interacting factors in the control of the Crustacean Molt cycle. Am Zool 25:275–284CrossRefGoogle Scholar
  133. Slusarczyk M (1995) Predator induced diapause in Daphnia. Ecology 76:1008–1013CrossRefGoogle Scholar
  134. Smirnov NN (1971) Chydoridae of the World. Nauka Academic Publishers, Leningrad (in Russian)Google Scholar
  135. Smyly WJP (1962) Laboratory experiments with stage V copepodids of the freshwater copepod, Cyclops leuckarti Claus, from Windemere and Easthwaite water. Crustaceana 4:273–280CrossRefGoogle Scholar
  136. Spectrova LV (1984) Recommendations for Artemia culturing and using in aquaculture. VINITI Center, Moscow, p N629px. [in Russian]Google Scholar
  137. Spindler KD (1971) Untersuchungen fiber den Einfiup auperer Faktoren auf die Darner der Embryonalentwicklung und der Hantungsrhythuns von Cyclops vicinus. Oecologia 7:342–355PubMedCrossRefGoogle Scholar
  138. Steele VJ (1981) The effect of photoperiod on the reproductive cycle of Gammarus lawrencianus Bousfield. J Exp Mar Biol Ecol 53:1–7CrossRefGoogle Scholar
  139. Stross RG (1965) Termination of summer and winter diapause in Daphnia. Am Zool 15:701Google Scholar
  140. Stross RG (1966) Light and temperature requirement for diapause development and release in Daphnia. Ecology 47:368–374CrossRefGoogle Scholar
  141. Stross RG (1969) Photoperiod control of diapause 142 in Daphnia. II. Induction of winter diapause in the arctic. Biol Bull 136:264–273CrossRefGoogle Scholar
  142. Stross RG (1971) Photoperiodism and diapause in Daphnia: a strategy for all seasons. Trans Am Microsc Soc 90:110–112Google Scholar
  143. Stross RG (1987) Photoperiodism and phased growth in Daphnia populations: coactions in perspective. In: Peters RH, de Bernardi R (eds) Daphnia. Memorie dell’Istituto Italiano di Idrobiologia, vol. 45, pp 413–437Google Scholar
  144. Stross RG, Chisholm SW (1975) Density stabilization in arctic populations of Daphnia. Verhandlungen Int Vereiningung Limnol 19:2879–2884Google Scholar
  145. Stross RG, Hill JC (1968) Photoperiod control of winter diapause in the fresh water Crustacean, Daphnia. Biol Bull 134:176–198CrossRefGoogle Scholar
  146. Stross RG, Kansas DA (1969) The reproductive cycle of Daphnia in an arctic pool. Ecology 50:457–460CrossRefGoogle Scholar
  147. Stuart C, Banta A (1931) Available bacteria and the sex ratio in Moina. Physiol Zool 4:654–696Google Scholar
  148. Tatar M, Bartke A, Antebi A (2003) The endocrine regulation of aging by insulin like signals. Science 299:1346–1351PubMedPubMedCentralCrossRefGoogle Scholar
  149. Tcherkashina NJA, Karnaushenko IV (1982) Before-embryonic diapause in cray-fish (Astacus leptodactilis cubanicus Bir. et Win.). J Obshej Biologii 43: 687–689 (in Russian)Google Scholar
  150. Thiriot A (1978) Zooplankton communities in the West African upwelling area. In: Boje R, Tomezak M (eds) Upwelling ecosystems. Springer, New YorkGoogle Scholar
  151. Tsukerzis JAM Shashtokas IA (1977) Embryonic diapause in the noble cray-fish (Astacus astacus L.). J Obshej Biologii 38: 929–933 (in Russian)Google Scholar
  152. Tunnecliffe A, Lapinski J, McGee B (2005) A Putative LEA protein, but no Trehalosa is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 542:315–321CrossRefGoogle Scholar
  153. Tyshchenko VP (1977) Fiziologiya fotoperiodizma u nasekomykh (Physiology of Photoperiodism in Insects). Nauka, Leningrad, 156 pp (In Russian)Google Scholar
  154. Ulomsky SN (1953) News in ecology of some Mesocyclops. Doklady Acad Sci USSR 90:295–297 (in Russian)Google Scholar
  155. Uye S, Kasahara S, Onbe T (1979) Calanoid copepod eggs in sea-bottom muds. IV. Effects of some environmental factors on the hatching of resting eggs. Mar Biol 51:151–156CrossRefGoogle Scholar
  156. Van den Bosch de Aguilar P (1969) Nouvelles Donnees Morphologiques et Hypothises sur le r61e du Systeme Neuro secreteue chez Daphnia pulex (Crustacea: Cladocera). Ann Soc R Zool Belgique 99:27–44Google Scholar
  157. Bertalanfy, L Von (1969) Study on common theory of systems. Progress, Moscow (in Russian)Google Scholar
  158. Watson NHF, Smallman BN (1971) The role of photoperiod and temperature in the induction and termination of an arrested development in two species of freshwater cyclopid copepods. Can J Zool 49:855–862CrossRefGoogle Scholar
  159. Weismann A (1880) Beitrage zur Naturgeschichteder Daphnoiden. Ztschr wiss Zool 33:55–270Google Scholar
  160. Westin L, Gydemo R (1986) Influence of light and temperature on reproduction and moulting frequency of the Crayfish Astacus astacus L. Aquaculture 52:43–50CrossRefGoogle Scholar
  161. Williams JA (1980) The light-response rhythm and seasonal entrainment of the endogenous circadian locomotor rhythm of Talitrus saltator (Crustacea, Amphipoda). J Mar Biol Assoc UK 60:773–785CrossRefGoogle Scholar
  162. Wilton DP, Smith GC (1985) Ovarian diapause in three geographic strains of Culex pipiens (Diptera, Culicidae). J Med Entomol 22:524–528PubMedCrossRefPubMedCentralGoogle Scholar
  163. Winberg GG (1936) Cyclic breeding in Cladocera. Usp Sovrem Biol 5:201–202 (in Russian)Google Scholar
  164. Wolkow CA, Kimura KD, Lee MS, Ruvkun G (2000) Regulation of C. elegans life span by insulin like signaling in the nervous system. Science 290:147–150CrossRefGoogle Scholar
  165. Woltereck R (1911) Ober Veranderung der Sexualitat Bei Daphniden. Int Rev Hydrobiol 4:91–128CrossRefGoogle Scholar
  166. Zaffagnini F (1987) Reproduction in Daphnia. Memorie dell’Istituto Italiano di Idrobiologia 45:245–284Google Scholar
  167. Zaslavsky VA (1988) Insect development. photoperiodic and temperature control. Springer, Berlin, p 187Google Scholar
  168. Zeleny N (1905) The relation of the degree of injury to the rate of regeneration. J Exp Zool 2:347–369CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Zoological Institute of Russian Academy of SciencesSt. PetersburgRussia
  2. 2.Laboratory of Experimental Entomology, Zoological Institute RASUniversity emb. 1St. PetersburgRussia

Personalised recommendations