1932

Abstract

Diapause is a type of dormancy that requires preparation, typically precedes the onset of unfavorable conditions, and necessitates a period of arrest before development can proceed. Two ecologically important groups of copepods have incorporated diapausing stages into their life histories. In freshwater, estuarine, and coastal environments, species within the Centropagoidea superfamily can produce resting eggs containing embryos that may be quiescent, diapausing, or in some intermediate state. Resting eggs sink into the sediments, remain viable over months to years, and form a reservoir from which the planktonic population is reestablished. In coastal and oceanic environments, copepods within the Calanidae and Eucalanidae families can enter diapause during late juvenile (copepodid) or adult stages. These copepods accumulate large amounts of lipids before they migrate into deep water and diapause for several months. Through respiration, diapausing copepods may sequester more carbon in the deep ocean than any other biogeochemical process, and changes in diapause phenology associated with climate change (particularly reduction in diapause duration) could have a significant impact not only on regional ecosystems, but on global climate as well.

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2017-01-03
2024-12-12
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Literature Cited

  1. Alekseev VR, Hwang J-S, Tseng M-H. 2006. Diapause in aquatic invertebrates: What's known and what's next in research and medical application?. J. Mar. Sci. Technol. 14:269–86 [Google Scholar]
  2. Alekseev VR, Lampert W. 2001. Maternal control of resting-egg production in Daphnia. Nature 414:899–901 [Google Scholar]
  3. Aruda AM, Baumgartner MF, Reitzel AM, Tarrant AM. 2011. Heat shock protein expression during stress and diapause in the marine copepod Calanus finmarchicus. J. Insect Physiol. 57:665–75 [Google Scholar]
  4. Atkinson A, Schnack-Schiel SB, Ward P, Marin V. 1997. Regional differences in the life cycle of Calanoides acutus (Copepoda: Calanoida) within the Atlantic sector of the Southern Ocean. Mar. Ecol. Prog. Ser. 150:99–111 [Google Scholar]
  5. Avery DE. 2005a. Induction of embryonic dormancy in the calanoid copepod Acartia hudsonica: heritability and phenotypic plasticity in two geographically separated populations. J. Exp. Mar. Biol. Ecol. 314:215–25 [Google Scholar]
  6. Avery DE. 2005b. Induction of embryonic dormancy in the calanoid copepod Acartia hudsonica: proximal cues and variation among individuals. J. Exp. Mar. Biol. Ecol. 314:203–14 [Google Scholar]
  7. Ban S. 1992a. Effects of photoperiod, temperature, and population density of induction of diapause egg production in Eurytemora affinis (Copepoda: Calanoida) in Lake Ohnuma, Hokkaido, Japan. J. Crustac. Biol. 12:361–67 [Google Scholar]
  8. Ban S. 1992b. Seasonal distribution, abundance, and viability of diapause eggs of Eurytemora affinis (Copepoda: Calanoida) in the sediment of Lake Ohnuma, Hokkaido. Bull. Plankton Soc. Jpn. 39:41–48 [Google Scholar]
  9. Ban S, Minoda T. 1991. The effect of temperature on the development and hatching of diapause and subitaneous eggs in Eurytemora affinis (Copepoda: Calanoida) in Lake Ohnuma, Hokkaido, Japan. Proceedings of the 4th International Conference on Copepoda ed. S-I Uye, S Nishida, J-S Ho 299–308 Bull. Plankton Soc. Jpn. Spec. Vol Tokyo: Plankton Soc. Jpn. [Google Scholar]
  10. Ban S, Minoda T. 1992. The hatching of diapause eggs of Eurytemora affinis (Copepoda: Calanoida) collected from lake-bottom sediments. J. Crustac. Biol. 12:51–56 [Google Scholar]
  11. Barthélémy R-M, Cuoc C, Defaye D, Brunet M, Mazza J. 1998. Female genital structures in several families of Centropagoidea (Copepoda: Calanoida). Philos. Trans. R. Soc. B 353:721–36 [Google Scholar]
  12. Bauermeister AEM, Sargent JR. 1979. Wax esters: major metabolites in the marine environment. Trends Biochem. Sci. 4:209–11 [Google Scholar]
  13. Beaugrand G, Luczak C, Edwards M. 2009. Rapid biogeographical plankton shifts in the North Atlantic Ocean. Glob. Change Biol. 15:1790–803 [Google Scholar]
  14. Belamonte G. 1992. Diapause egg production in Acartia (Paracartia) latisetosa (Crustacea, Copepoda, Calanoida). Boll. Zool. 59:363–66 [Google Scholar]
  15. Berasategui AA, Hoffmeyer MS, Dutto MS, Biancalana F. 2012. Seasonal variation in the egg morphology of the copepod Eurytemora americana and its relationship with reproductive strategy in a temperate estuary in Argentina. ICES J. Mar. Sci. 69:380–88 [Google Scholar]
  16. Berenike A, Diekmann S, Clemmesen C, St. John MA, Paulsen M, Peck MA. 2012. Environmental cues and constraints affecting the seasonality of dominant calanoid copepods in brackish, coastal waters: a case study of Acartia, Temora and Eurytemora species in the south-west Baltic. Mar. Biol. 159:2399–414 [Google Scholar]
  17. Blades-Eckelbarger PI. 1991. Comparative ultrastructure of lipid storage sites in female Euchaeta marina and Pleuromamma xiphias (Copepoda: Calanoida). Mar. Biol. 108:49–58 [Google Scholar]
  18. Bozelli RL, Tonsi M, Sandrini F, Manca M. 2008. A big bang or small bangs? Effects of biotic environment on hatching. J. Limnol. 67:100–6 [Google Scholar]
  19. Buesseler KO, Lamborg CH, Boyd PW, Lam PJ, Trull TW. et al. 2007. Revisiting carbon flux through the ocean's twilight zone. Science 316:567–70 [Google Scholar]
  20. Campbell RW, Boutillier P, Dower JF. 2004. Ecophysiology of overwintering in the copepod Neocalanus plumchrus: changes in lipid and protein contents over a seasonal cycle. Mar. Ecol. Prog. Ser. 280:211–26 [Google Scholar]
  21. Campbell RW, Dower JF. 2003. Role of lipids in the maintenance of neutral buoyancy by zooplankton. Mar. Ecol. Prog. Ser. 263:93–99 [Google Scholar]
  22. Carstensen J, Weydmann A, Olszewska A, Kawsniewski S. 2012. Effects of environmental conditions on the biomass of Calanus spp. in the Nordic Seas. J. Plankton Res. 34:951–66 [Google Scholar]
  23. Castro-Longoria E, Williams JA. 1999. The production of subitaneous and diapause eggs: a reproductive strategy for Acartia bifilosa (Copepoda: Calanoida) in Southampton Water, UK. J. Plankton Res. 21:65–84 [Google Scholar]
  24. Chen F, Marcus NH. 1997. Subitaneous, diapause, and delayed-hatching eggs of planktonic copepods from the northern Gulf of Mexico: morphology and hatching success. Mar. Biol. 127:587–97 [Google Scholar]
  25. Chust G, Castellani C, Licandro P, Ibaibarriaga L, Sagarminaga Y, Irigoien X. 2014. Are Calanus spp. shifting poleward in the North Atlantic? A habitat modeling approach. ICES J. Mar. Sci. 71:241–53 [Google Scholar]
  26. Clarke MR, Denton EJ, Gilpin-Brown JB. 1979. On the use of ammonium for buoyancy in squids. J. Mar. Biol. Assoc. UK 59:259–76 [Google Scholar]
  27. Conover RJ. 1965. Notes on the molting cycle, development of sexual characteristics and sex ratio in Calanus hyperboreus. Crustaceana 8:308–20 [Google Scholar]
  28. Coull BC, Grant J. 1981. Encystment discovered in a marine copepod. Science 212:342–44 [Google Scholar]
  29. Crain J, Miller C. 2000. Detection of sex and sex ratio in Calanus finmarchicus early stage fifth copepodites. ICES J. Mar. Sci. 57:1773–79 [Google Scholar]
  30. Dahms H. 1995. Dormancy in the Copepoda—an overview. Hydrobiologia 306:199–211 [Google Scholar]
  31. Danks HV. 1987. Insect Dormancy: An Ecological Perspective Gloucester, Can.: Tyrell Press [Google Scholar]
  32. Denlinger D. 2002. Regulation of diapause. Annu. Rev. Entomol. 47:93–122 [Google Scholar]
  33. Drillet G, Hansen BW, Kiorboe T. 2011. Resting egg production induced by food limitation in the calanoid copepod Acartia tonsa. Limnol. Oceanogr. 56:2064–70 [Google Scholar]
  34. Durbin EG, Garrahan P, Casas M. 2000. Abundance and distribution of Calanus finmarchicus on the Georges Bank during 1995 and 1996. ICES J. Mar. Sci. 57:1664–85 [Google Scholar]
  35. Durbin EG, Runge JA, Campbell RG, Garrahan PR, Casas MC, Plourde S. 1997. Late fall-early winter recruitment of Calanus finmarchicus on Georges Bank. Mar. Ecol. Prog. Ser. 151:103–14 [Google Scholar]
  36. Engel M, Hirche H-J. 2004. Seasonal variability and interspecific difference in hatching of calanoid copepod resting eggs from sediments of the German Bight (North Sea). J. Plankton Res. 9:1083–93 [Google Scholar]
  37. Fiksen Ø. 2000. The adaptive timing of diapause—a search for evolutionarily robust strategies in Calanus finmarchicus. ICES J. Mar. Sci. 57:1825–33 [Google Scholar]
  38. Fujiwara Y, Tanaka Y, Iwata K, Rubio RO, Yaginuma T. et al. 2006. ERK/MAPK regulates ecdysteroid and sorbitol metabolism for embryonic diapause termination in the silkworm, Bombyx mori. J. Insect Physiol. 52:569–75 [Google Scholar]
  39. Fulton J. 1973. Some aspects of the life history of Calanus plumchrus in the Strait of Georgia. J. Fish. Res. Board Can. 30:811–15 [Google Scholar]
  40. Glippa O, Souissi S, Denis L, Lesourd S. 2011. Calanoid copepod resting egg abundance and hatching success in the sediment of the Seine estuary (France). Estuar. Coast. Shelf Sci. 92:255–62 [Google Scholar]
  41. Grice GD. 1956. A qualitative and quantitative seasonal study of the Copepoda of Alligator Harbor. Fla. State Univ. Stud. 22:37–76 [Google Scholar]
  42. Grigg H, Bardwell SJ. 1982. Seasonal observations on moulting and maturation in stage V copepodites of Calanus finmarchicus from the Firth of Clyde. J. Mar. Biol. Assoc. UK 69:315–27 [Google Scholar]
  43. Gyllström M, Hansson L-A. 2004. Dormancy in freshwater zooplankton: induction, termination and the importance of benthic-pelagic coupling. Aquat. Sci. 66:274–95 [Google Scholar]
  44. Hairston NG Jr.. 1996. Zooplankton egg banks as biotic reservoirs in changing environments. Limnol. Oceanogr. 41:1087–92 [Google Scholar]
  45. Hairston NG Jr., Hansen A-M, Schaffner WR. 2000. The effect of diapause emergence on the seasonal dynamics of a zooplankton assemblage. Freshw. Biol. 45:133–45 [Google Scholar]
  46. Hairston NG Jr., Kearns CM. 1995. The interaction of photoperiod and temperature in diapause timing: a copepod example. Biol. Bull. 189:42–48 [Google Scholar]
  47. Hairston NG Jr., Olds EJ. 1986. Partial photoperiodic control of diapause in three populations of the freshwater copepod Diaptomus sanguineus. Biol. Bull. 171:135–42 [Google Scholar]
  48. Hairston NG Jr., Van Brunt RA. 1994. Diapause dynamics of two diaptomid copepod species in a large lake. Hydrobiologia 292/93:209–18 [Google Scholar]
  49. Hallberg E, Hirche H-J. 1980. Differentiation of mid-gut in adults and over-wintering copepodid of Calanus finmarchicus (Gunnerus) and C. helgolandicus Claus. J. Exp. Mar. Biol. Ecol. 48:283–95 [Google Scholar]
  50. Hand SC, Menze MA, Borcar A, Patil Y, Covi JA. et al. 2011. Metabolic restructuring during energy-limited states: insights from Artemia franciscana embryos and other animals. J. Insect Physiol. 57:584–94 [Google Scholar]
  51. Hansen BW, Drillet G. 2013. Comparative oxygen consumption rates of subitaneous and delayed hatching eggs of the calanoid copepod Acartia tonsa (Dana). J. Exp. Mar. Biol. Ecol. 442:66–69 [Google Scholar]
  52. Hansen BW, Drillet G, Pedersen MF, Sjøgreen KP, Vismann B. 2012. Do Acartia tonsa (Dana) eggs regulate their volume and osmolality as salinity changes?. J. Comp. Physiol. B 182:613–23 [Google Scholar]
  53. Head E, Pepin P. 2007. Variations in overwintering depth distributions of Calanus finmarchicus in the slope waters of the NW Atlantic continental shelf and the Labrador Sea. J. Northwest Atl. Fish. Sci. 39:49–69 [Google Scholar]
  54. Heath MR, Fraser JG, Gislason A, Hay SJ, Jónasdóttir SH, Richardson K. 2000. Winter distribution of Calanus finmarchicus in the Northeast Atlantic. ICES J. Mar. Sci. 57:1628–35 [Google Scholar]
  55. Helaouet P, Beaugrand G. 2007. Macroecology of Calanus finmarchicus and C. helgolandicus in the North Atlantic Ocean and adjacent seas. Mar. Ecol. Prog. Ser. 345:147–65 [Google Scholar]
  56. Hind A, Gurney W, Heath M, Bryant A. 2000. Overwintering strategies of Calanus finmarchicus. Mar. Ecol. Prog. Ser. 193:95–107 [Google Scholar]
  57. Hirche H-J. 1983. Overwintering of Calanus finmarchicus and Calanus helgolandicus. Mar. Ecol. Prog. Ser. 11:281–90 [Google Scholar]
  58. Hirche H-J. 1991. Distribution of dominant calanoid copepod species in the Greenland sea during late fall. Polar Biol. 11:351–62 [Google Scholar]
  59. Hirche H-J. 1996. Diapause in the marine copepod, Calanus finmarchicus—a review. Ophelia 44:129–43 [Google Scholar]
  60. Hirche H-J. 1997. Life cycle of the copepod Calanus hyperboreus in the Greenland Sea. Mar. Biol. 128:607–18 [Google Scholar]
  61. Holtz RB, Marques ED, Benson AA. 1973. Wax ester biosynthesis by isolated membrane fractions from calanoid copepods. Comp. Biochem. Physiol. B 45:585–91 [Google Scholar]
  62. Ianora A, Santella L. 1991. Diapause embryos in the neustonic copepod Anomalocera patersoni. Mar. Biol. 108:387–95 [Google Scholar]
  63. Ingvarsdóttir A, Houlihan DF, Heath MR, Hay SJ. 1999. Seasonal changes in respiration rates of copepodite stage V Calanus finmarchicus (Gunnerus). Fish. Oceanogr. 8:73–83 [Google Scholar]
  64. Irigoien X. 2004. Some ideas about the role of lipids in the life cycle of Calanus finmarchicus. J. Plankton Res. 26:259–63 [Google Scholar]
  65. Ji R, Ashjian CJ, Campbell RG, Chen C, Gao G. et al. 2012. Life history and biogeography of Calanus copepods in the Arctic Ocean: an individual-based modeling study. Prog. Oceanogr. 96:40–56 [Google Scholar]
  66. Johnson CL. 2004. Seasonal variation in the molt status of an oceanic copepod. Prog. Oceanogr. 62:15–32 [Google Scholar]
  67. Johnson CL, Checkley DM Jr. 2004. Vertical distribution of diapausing Calanus pacificus (Copepoda) and implications for transport in the California undercurrent. Prog. Oceanogr. 62:1–13 [Google Scholar]
  68. Johnson CL, Leising AW, Runge JA, Head EJH, Pepin P. et al. 2008. Characteristics of Calanus finmarchicus dormancy patterns in the Northwest Atlantic. ICES J. Mar. Sci. 65:339–50 [Google Scholar]
  69. Jónasdóttir SH. 1999. Lipid content of Calanus finmarchicus during overwintering in the Faroe–Shetland Channel. Fish. Oceanogr. 8:61–72 [Google Scholar]
  70. Jónasdóttir SH, Vissir AW, Richardson K, Heath MR. 2015. Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic. PNAS 112:12122–26 [Google Scholar]
  71. Katajisto T. 2006. Benthic resting eggs in the life cycles of calanoid copepods in the northern Baltic Sea Sci. Rep. 29 Walter Andrée de Nottbeck Found. Helsinki: [Google Scholar]
  72. King AM, MacRae TH. 2015. Insect heat shock proteins during stress and diapause. Annu. Rev. Entomol. 60:59–75 [Google Scholar]
  73. Kobari T, Ikeda T. 1999. Vertical distribution, population structure and life cycle of Neocalanus cristatus (Crustacea: Copepoda) in the Oyashio region, with notes on its regional variations. Mar. Biol. 134:683–96 [Google Scholar]
  74. Kobari T, Ikeda T. 2001a. Life cycle of Neocalanus flemingeri (Crustacea: Copepoda) in the Oyashio region, western subarctic Pacific, with notes on its regional variations. Mar. Ecol. Prog. Ser. 209:243–55 [Google Scholar]
  75. Kobari T, Ikeda T. 2001b. Ontogenetic vertical migration and life cycle of Neocalanus plumchrus (Crustacea: Copepoda) in the Oyashio region, with notes on regional variations in body size. J. Plankton Res. 23:287–302 [Google Scholar]
  76. Koštál V. 2006. Eco-physiological phases of insect diapause. J. Insect Physiol. 52:113–27 [Google Scholar]
  77. Larade K, Storey KB. 2004. Accumulation and translation of ferritin heavy chain transcripts following anoxia exposure in a marine invertebrate. J. Exp. Biol. 207:1353–60 [Google Scholar]
  78. LeBour MV. 1916. Stages in the life history of Calanus finmarchicus (Gunnerus), experimentally reared by Mr. L. R. Crawshay in the Plymouth Laboratory. J. Mar. Biol. Assoc. UK 11:1–17 [Google Scholar]
  79. Lee RF, Hagen W, Kattner G. 2006. Lipid storage in marine zooplankton. Mar. Ecol. Prog. Ser. 307:273–306 [Google Scholar]
  80. Lindley JA. 1990. Distribution of overwintering calanoid copepods in sea-bed sediments around southern Britain. Mar. Biol. 104:209–17 [Google Scholar]
  81. Longhurst A, Sameoto D, Herman A. 1984. Vertical distribution of zooplankton in summer: eastern Canadian archipelago. J. Plankton Res. 6:137–68 [Google Scholar]
  82. MacRae TH. 2016. Stress tolerance during diapause and quiescence of the brine shrimp, Artemia. Cell Stress Chaperones 21:9–18 [Google Scholar]
  83. Madhupratap M, Nehring S, Lenz J. 1996. Resting eggs of zooplankton (Copepoda and Cladocera) from the Kiel Bay and adjacent waters (southwestern Baltic). Mar. Biol. 125:77–87 [Google Scholar]
  84. Maps F, Plourde S, Zakardjian B. 2010. Control of dormancy by lipid metabolism in Calanus finmarchicus: a population test model. Mar. Ecol. Prog. Ser. 403:165–80 [Google Scholar]
  85. Maps F, Record NR, Pershing AJ. 2014. A metabolic approach to dormancy in pelagic copepods helps explaining inter- and intra-specific variability in life-history strategies. J. Plankton Res. 36:18–30 [Google Scholar]
  86. Maps F, Runge JA, Leising A, Pershing AJ, Record NR. et al. 2012. Modelling the timing and duration of dormancy in populations of Calanus finmarchicus from the Northwest Atlantic shelf. J. Plankton Res. 34:36–54 [Google Scholar]
  87. Marcus NH. 1979. On the population biology and nature of diapause of Labidocera aestiva (Copepoda: Calanoida). Biol. Bull. 157:297–305 [Google Scholar]
  88. Marcus NH. 1982. Photoperiodic and temperature regulation of diapause in Labidocera aestiva (Copepoda: Calanoida). Biol. Bull. 162:45–52 [Google Scholar]
  89. Marcus NH. 1984. Recruitment of copepod nauplii into the plankton: importance of diapause eggs and benthic processes. Mar. Ecol. Prog. Ser. 15:47–54 [Google Scholar]
  90. Marcus NH. 1987. Differences in the duration of egg diapause of Labidocera aestiva (Copepoda: Calanoida) from the Woods Hole, Massachusetts, region. Biol. Bull. 173:169–77 [Google Scholar]
  91. Marcus NH. 1989. Abundance in bottom sediments and hatching requirements of eggs of Centropages hamatus (Copepoda: Calanoida) from the Alligator Harbor region, Florida. Biol. Bull. 176:142–46 [Google Scholar]
  92. Marcus NH. 1996. Ecological and evolutionary significance of resting eggs in marine copepods: past, present, and future studies. Hydrobiologia 320:141–52 [Google Scholar]
  93. Marcus NH. 2004. An overview of the impacts of eutrophication and chemical pollutants on copepods of the coastal zone. Zool. Stud. 43:211–17 [Google Scholar]
  94. Marcus NH, Lutz R, Burnett W, Cable P. 1994. Age, viability, and vertical distribution of zooplankton resting eggs from an anoxic basin: evidence of an egg bank. Limnol. Oceanogr. 39:154–58 [Google Scholar]
  95. Marcus NH, Lutz RV. 1998. Longevity of subitaneous and diapause eggs of Centropages hamatus (Copepoda: Calanoida) from the northern Gulf of Mexico. Mar. Biol. 131:249–57 [Google Scholar]
  96. Mayor DJ, Sommer U, Cook KB, Viant MR. 2015. The metabolic response of marine copepods to environmental warming and ocean acidification. Sci. Rep. 5:13690 [Google Scholar]
  97. McLaren IA, Head E, Sameoto DD. 2001. Life cycles and seasonal distributions of Calanus finmarchicus on the central Scotian Shelf. Can. J. Fish. Aquat. Sci. 58:659–70 [Google Scholar]
  98. Miller CB, Clemons MJ. 1988. Revised life history analysis for large grazing copepods in the subarctic Pacific Ocean. Prog. Oceanogr. 20:293–313 [Google Scholar]
  99. Miller CB, Cowles TJ, Wiebe PH, Copley NJ, Grigg H. 1991. Phenology in Calanus finmarchicus; hypotheses about control mechanisms. Mar. Ecol. Prog. Ser. 72:79–91 [Google Scholar]
  100. Miller CB, Frost BW, Batchelder HP, Clemons MJ, Conway RE. 1984. Life histories of large, grazing copepods in a subarctic ocean gyre: Neocalanus plumchrus, Neocalanus cristatus, and Eucalanus bungii in the Northeast Pacific. Prog. Oceanogr. 13:201–43 [Google Scholar]
  101. Miller CB, Morgan CA, Prahl FG, Sparrow MA. 1998. Storage lipids of the copepod Calanus finmarchicus from Georges Bank and the Gulf of Maine. Limnol. Oceanogr. 43:488–97 [Google Scholar]
  102. Miller CB, Nelson DM, Weiss C, Soeldner AH. 1990. Morphogenesis of opal teeth in calanoid copepods. Mar. Biol. 106:91–101 [Google Scholar]
  103. Ohman MD, Drits AV, Clarke ME, Plourde S. 1998. Differential dormancy of co-occurring copepods. Deep-Sea Res. II 45:1709–40 [Google Scholar]
  104. Osgood KE, Checkley DM Jr.. 1997. Observations of a deep aggregation of Calanus pacificus in the Santa Barbara Basin. Limnol. Oceanogr. 42:997–1001 [Google Scholar]
  105. Papanastaiou SA, Nestel D, Diamantidis AD, Nakas CT, Papadopoulos NT. 2011. Physiological and biological patterns of a highland and a coastal population of the European cherry fruit fly during diapause. J. Insect Physiol. 57:83–93 [Google Scholar]
  106. Pierson JJ, Batchelder H, Saumweber W, Leising A, Runge J. 2013. The impact of increasing temperatures on dormancy duration in Calanus finmarchicus. J. Plankton Res. 35:504–12 [Google Scholar]
  107. Pijanowska J, Stolpe G. 1996. Summer diapause in Daphnia as a reaction to the presence of fish. J. Plankton Res. 18:1407–12 [Google Scholar]
  108. Plourde S, Runge JA. 1993. Reproduction of the planktonic copepod Calanus finmarchicus in the Lower St. Lawrence Estuary: relation to the cycle of phytoplankton production and evidence for a Calanus pump. Mar. Ecol. Prog. Ser. 102:217–27 [Google Scholar]
  109. Podrabsky JE, Hand SC. 2015. Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish. J. Exp. Biol. 218:1897–906 [Google Scholar]
  110. Pond DW. 2012. The physiological properties of lipids and their role in controlling the distribution of zooplankton in the oceans. J. Plankton Res. 34:443–53 [Google Scholar]
  111. Pond DW, Tarling GA. 2011. Phase transitions of wax esters adjust buoyancy in diapausing Calanoides acutus. Limnol. Oceanogr. 56:1310–18 [Google Scholar]
  112. Radizikowski J. 2013. Resistance of dormant stages of planktonic invertebrates to adverse environmental conditions. J. Plankton Res. 35:707–23 [Google Scholar]
  113. Rey-Rassat C, Irigoien X, Harris R, Head R, Carlotti F. 2002. Growth and development of Calanus helgolandicus reared in the laboratory. Mar. Ecol. Prog. Ser. 238:125–38 [Google Scholar]
  114. Reynolds JA, Hand SC. 2009. Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket Allonemobius socius. J. Exp. Biol. 212:2075–84 [Google Scholar]
  115. Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SAL, Denlinger DL. 2007. Up-regulation of heat shock proteins is essential for cold survival during insect diapause. PNAS 104:11130–37 [Google Scholar]
  116. Romano G, Ianora A, Miralto A. 1996a. Respiratory physiology in summer diapause embryos of the neustonic copepod Anomalocera patersoni. Mar. Biol. 127:229–34 [Google Scholar]
  117. Romano G, Ianora A, Santella L, Miralto A. 1996b. Respiratory metabolism during embryonic subitaneous and diapause development in Pontella mediterranea (Crustacea: Copepoda). J. Comp. Physiol. B 166:157–63 [Google Scholar]
  118. Roulin AC, Routtu J, Hall MD, Janicke T, Colson I. et al. 2013. Local adaptation of sex induction in a facultative sexual crustacean: insights from QTL mapping and natural populations of Daphnia magna. Mol. Ecol. 22:3567–79 [Google Scholar]
  119. Sameoto DD, Herman AW. 1990. Life cycle and distribution of Calanus finmarchicus in deep basins on the Nova Scotia shelf and seasonal changes in Calanus spp. Mar. Ecol. Prog. Ser. 66:225–37 [Google Scholar]
  120. Sanders NK, Childress JJ. 1988. Ion replacement as a buoyancy mechanism in a pelagic deep-sea crustacean. J. Exp. Biol. 138:333–43 [Google Scholar]
  121. Sars GO. 1903. An Account of the Crustacea of Norway Bergen, Nor.: Bergen Mus. [Google Scholar]
  122. Sartoris FJ, Thomas DN, Cornils A, Schnack-Schiel SB. 2010. Buoyancy and diapause in Antarctic copepods: the role of ammonium accumulation. Limnol. Oceanogr. 55:1860–64 [Google Scholar]
  123. Saumweber WJ, Durbin EG. 2006. Estimating potential diapause duration in Calanus finmarchicus. Deep-Sea Res. II 53:2597–617 [Google Scholar]
  124. Schröder T. 2005. Diapause in monogonont rotifers. Hydrobiologia 546:291–306 [Google Scholar]
  125. Schröder T, Gilbert JJ. 2004. Trangenerational plasticity for sexual reproduction and diapause in the life cycle of monogonont rotifers: intraclonal, intraspecific and interspecific variation in the response to crowding. Funct. Ecol. 18:458–66 [Google Scholar]
  126. Schründer S, Schnack-Schiel SB, Auel H, Sartoris FJ. 2013. Control of diapause by acidic pH and ammonium accumulation in the haemolymph of Antarctic copepods. PLOS ONE 8:e77498 [Google Scholar]
  127. Sgolastra F, Bosch J, Molowny-Horas R, Maini S, Kemp WP. 2010. Effect of temperature regime on diapause intensity in an adult-wintering Hymenopteran with obligate diapause. J. Insect Physiol. 56:185–94 [Google Scholar]
  128. Ślusarczyk M, Rygielska E. 2004. Fish faeces as the primary source of chemical cues inducing fish avoidance diapause in Daphnia magna. Hydrobiologia 526:231–34 [Google Scholar]
  129. Smith SL. 1990. Egg production and feeding by copepods prior to the spring bloom of phytoplankton in the Fram Strait area of the Greenland Sea. Mar. Biol. 106:59–69 [Google Scholar]
  130. Søreide JE, Leu E, Berge J, Graeve M, Falk-Petersen S. 2010. Timing of blooms, algal food quality and Calanus glacialis reproduction and growth in a changing Arctic. Glob. Change Biol. 16:3154–63 [Google Scholar]
  131. Speirs DC, Gurney WS, Heath MR, Wood SN. 2005. Modelling the basin-scale demography of Calanus finmarchicus in the north-east Atlantic. Fish. Oceanogr 14:333–58 [Google Scholar]
  132. Stross RG, Hill JC. 1965. Diapause induction in Daphnia requires two stimuli. Science 150:1463–64 [Google Scholar]
  133. Sullivan BK, Costello JH, Van Keuren D. 2007. Seasonality of the copepods Acartia hudsonica and Acartia tonsa in Narragansett Bay, RI, USA during a period of climate change. Estuar. Coast. Shelf Sci. 73:259–67 [Google Scholar]
  134. Sullivan BK, McMannus LT. 1986. Factors controlling seasonal succession of the copepods Acartia hudsonica and A. tonsa in Narragansett Bay, Rhode Island: temperature and resting egg production. Mar. Ecol. Prog. Ser. 28:121–28 [Google Scholar]
  135. Tande KS. 1982. Ecological investigations on the zooplankton community of Balsfjorden, northern Norway: generation cycles, and variations in body weight and body content of carbon and nitrogen related to overwintering and reproduction in the copepod Calanus finmarchicus (Gunnerus). J. Exp. Mar. Biol. Ecol. 62:129–42 [Google Scholar]
  136. Tande KS, Slagstad D. 1982. Ecological investigation on the zooplankton community of Balsfjorden, northern Norway: seasonal and short-time variations in enzyme activity in copepodite stage V and VI males and females of Calanus finmarchicus (Gunnerus). Sarsia 67:63–68 [Google Scholar]
  137. Tarrant AM, Baumgartner MF, Lysiak NSJ, Altin D, Størseth TR, Hansen BH. 2016. Transcriptional profiling of metabolic transitions during development and diapause preparation in the copepod Calanus finmarchicus. Integr. Comp. Biol. In press. doi: 10.1093/icb/icw060 [Google Scholar]
  138. Tarrant AM, Baumgartner MF, Verslycke T, Johnson C. 2008. Differential gene expression in diapausing and active Calanus finmarchicus (Copepoda). Mar. Ecol. Prog. Ser. 355:193–207 [Google Scholar]
  139. Thomas AC, Townsend DW, Weatherbee R. 2003. Satellite-measured phytoplankton variability in the Gulf of Maine. Cont. Shelf Res. 23:971–89 [Google Scholar]
  140. Tittensor DP, DeYoung B, Tang CL. 2003. Modelling the distribution, sustainability and diapause emergence timing of the copepod Calanus finmarchicus in the Labrador Sea. Fish. Oceanogr. 12:299–316 [Google Scholar]
  141. 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. Res. 51:151–56 [Google Scholar]
  142. Varpe O, Jorgensen C, Tarling GA, Fiksen O. 2009. The adaptive value of energy storage and capital breeding in seasonal environments. Oikos 118:363–70 [Google Scholar]
  143. Visser AW, Jónasdóttir SH. 1999. Lipids, buoyancy and the seasonal vertical migration of Calanus finmarchicus. Fish. Oceanogr 8:100–6 [Google Scholar]
  144. Wagner M, Campbell R, Boudreau C, Durbin E. 2001. Nucleic acids and growth of Calanus finmarchicus in the laboratory under different food and temperature conditions. Mar. Ecol. Prog. Ser. 221:185–97 [Google Scholar]
  145. Williams R, Conway VP. 1988. Vertical distribution and seasonal numerical abundance of the Calanidae in oceanic waters to the south-west of the British Isles. Hydrobiologia 167:259–66 [Google Scholar]
  146. Wu L-S, Wang G-Z, Li S-H. 2009. The differences in metabolic activity of subitaneous and diapause eggs in Centropages tenuiremis. J. Plankton Res. 31:223c31 [Google Scholar]
  147. Yayanos AA, Benson AA, Nevenzel JC. 1978. The pressure-volume-temperature (PVT) properties of a lipid mixture from a marine copepod, Calanus plumchrus: implications for buoyancy and sound scattering. Deep-Sea Res 25:257–68 [Google Scholar]
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