, Volume 320, Issue 1–3, pp 141–152 | Cite as

Ecological and evolutionary significance of resting eggs in marine copepods: past, present, and future studies

  • Nancy H. Marcus
The Nature of Resting Stages and their Role in the Population Dynamics of Marine and Freshwater Crustaceans


The occurrence of a resting egg phase in the life cycle of marine and freshwater planktonic copepods is well documented and receiving increasing attention by investigators. The species generally occur in coastal marine waters, freshwater ponds and lakes in areas that undergo strong seasonal fluctuations, though examples have been reported for tropical and sub-tropical areas not subject to such extreme fluctuations. Typically such species disappear from the water column for portions of the year, but remain in the region as benthic resting eggs. Studies to date have focused on the conditions that promote the occurrence of resting eggs, the factors that affect their survival and hatching from sediments, the existence of egg banks in sediments, and the impact of resting eggs on plankton community structure. Benthic resting eggs of copepods include diapause eggs as well as subitaneous (non-diapause) eggs that are quiescent due to conditions in the sediments. As with other groups of organisms the resting egg phase is viewed as being critical for the perpetuation of species year after year, especially those that disappear from the water column for portions of the year. Some data indicate that eggs can survive for many years in sediments which would expand their influence to evolutionary time scales. This paper summarizes our understanding of embryonic dormancy in marine copepods.

Key words

Copepod dormancy diapause resting eggs 


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  1. Alekseev, V., 1990. Diapauza rakoobraznykh: Ekologicheskiye i fiziologicheskiye aspekty (Diapause in Crustaceans: Ecological and Physiological Aspects). Nauka Press, Moscow, 143 pp.Google Scholar
  2. Ban, S., 1992a. Effects of photoperiod, temperature, and population density on induction of diapause egg production in Eurytemora affinis (Copepoda:calanoida) in Lake Ohnuma, Hokkaido, Japan. J. Crust. Biol. 12: 361–367.Google Scholar
  3. Ban, S., 1992b. Seasonal distribution, abundance, and viability of diapause eggs of Eurytemora affinis (Copepoda:Calanoida) in the sediment of Lake Ohnuma, Hokkaido. Bull. Plank. Soc. Japan 39: 41–48.Google Scholar
  4. Ban, S. & T. Minoda, 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. Bull. Plank. Soc. Japan, Spec. Vol.: 299–308.Google Scholar
  5. Ban, S. & T. Minoda, 1992. Hatching of diapause eggs of Eurytemora affinis (Copepoda:Calanoida) collected from lake-bottom sediments. J. Crust. Biol. 12: 51–56.Google Scholar
  6. Belmonte, G., 1992. Diapause egg production in Acartia (Paracartia) latisetosa (Crustacea, Copepoda, Calanoida). Boll. Zool. 59: 363–366.Google Scholar
  7. Boileau, M. G. & P. D. N. Hebert, 1991. Genetic consequences of passive dispersal in pond-dwelling copepods. Evolution 45: 721–733.Google Scholar
  8. Brewer, R. H., 1964. The phenology of Diaptomus stagnalis (Copepods:Calanoida): the development and hatching of the egg stage. Physiol. Zool. 37: 1–20.Google Scholar
  9. Chen, F. & S.-J. Li, 1991. On seasonal distribution and diapause eggs in Tortanus from Xiamen waters. Acta Oceanologica Sinica 13: 721–727. (Chinese).Google Scholar
  10. Chen, F. & S.-J. Li, 1992. Seasonal variation of two physiological types of Tortanus eggs from Xiamen waters, and their temperature effect. J. appl. Ecol. 3: 62–68. (In Chinese with English summary).Google Scholar
  11. Corner, E. & S. O'Hara, 1986. The Biological Chemistry of Copepods. Clarendon Press, Oxford.Google Scholar
  12. Coull, B. & J. Grant, 1981. Encystment discovered in a marine copepod. Science 212: 342.Google Scholar
  13. Danilevsky, A., 1965. Photoperiodism and Seasonal Development of Insects. 1st English Edition. Oliver & Boyd, Edinburgh.Google Scholar
  14. Danks, H. V., 1987. Insect Dormancy: An Ecological Perspective. Tyrell Press, Gloucester, 439 pp.Google Scholar
  15. Davis, C. C., 1984. Planktonic Copepoda (including Monstrilloida). pp. 67–91. In, Marine Plankton Life Cycle Strategies. K. A. Steidinger and L. M. Walker (eds), CRC Press, Boca Raton.Google Scholar
  16. De Stasio Jr., B. T., 1989. The seed bank of a freshwater crustacean: copepodology for the plant ecologist. Ecology 70: 1377–1389.Google Scholar
  17. Elgmork, K., 1980. Evolutionary aspects of diapause in freshwater copepods. pp. 411–417. In, Evolution and Ecology of Zooplankton Communities. W. C. Kerfoot (ed.). University Press of New England, Hanover.Google Scholar
  18. Fanelli, G., A. Ianora & L. Santella, 1992. Produzione de uova di diapausa nel ciclo biologico del copepode Acartia latisetosa (Kriczaguin). Oebelia suppl, XVII: 295–302.Google Scholar
  19. Grice, G. D. & V. Gibson, 1977. Resting eggs in Pontella meadi (Copepoda:Calanoida). J. Fish. Res. Bd Can. 34: 410–412.Google Scholar
  20. Grice, G. D. & V. Gibson, 1981. Hatching of eggs of Pontella mediterranea Claus (Copepoda:Calanoida). Vie Milieu 31: 49–51.Google Scholar
  21. Grice, G. D. & T. J. Lawson, 1976. Resting eggs in the marine calanoid copepod, Labidocera aestiva Wheeler. Crustaceana 30: 9–12.Google Scholar
  22. Grice, G. D. & N. H. Marcus, 1981. Dormant eggs of marine copepods. Oceanogr. Mar. Biol. annu. Rev. 19: 125–140.Google Scholar
  23. Hairston Jr., N. G. & B. T. De Stasio Jr., 1984. Rate of evolution slowed by a dormant propagule pool. Nature. 336: 239–242.Google Scholar
  24. Hairston Jr., N. G. & W. R. Munns Jr., 1984. The timing of copepod diapause as an evolutionary stable strategy. American Naturalist 123: 733–751.Google Scholar
  25. Hairston Jr., N. G. & E. J. Olds, 1984. Population differences in the timing of diapause:adaptation in a spatially heterogenous environment. Oecologia (Berlin) 61: 42–48.Google Scholar
  26. Hairston Jr., N. G. & E. J. Olds, 1987. Population differences in the timing of diapause: a test of hypotheses. Oecologia 71: 339–344.Google Scholar
  27. Hairston Jr., N. G., E. J. Olds & W. R. Munns Jr., 1985. Bet-hedging and environmentally cued diapause strategies of diaptomid copepods. International Vereinigung fur Theoretische und angewandte Limnologie, Verhandlungen 22: 3170- 3177.Google Scholar
  28. Hairston Jr., N. G. & W. E. Walton, 1986. Rapid evolution of a life history trait. Proc. natn. Acad. Sci. USA 83: 4831–4833.Google Scholar
  29. Huys, R. & G. A. Boxshall, 1991. Copepod Evolution. The Ray Society, London, 468 pp.Google Scholar
  30. Ianora, A. & L. Santella, 1991. Diapause embryos in the neustonic copepod Anomalocera patersoni. Mar. Biol. 108: 387–395.Google Scholar
  31. Johnson, J. K., 1980. Effects of temperature and salinity on production and hatching of dormant eggs of Acartia californiensis (Copepoda) in an Oregon estuary. Fish. Bull. 77: 567–584.Google Scholar
  32. Kasahara, S., S. Uye & T. Onbe, 1974. Calanoid copepod eggs in sea-bottom muds. Mar. Biol. 26: 167–171.Google Scholar
  33. Kasahara, S., S. Uye & T. Onbe, 1975. Calanoid copepod eggs in sea-bottom muds. II. Seasonal cycles of abundance in the populations of several species of copepods and their eggs in the Inland Sea of Japan. Mar. Biol. 31: 25–29.Google Scholar
  34. Landry, M. R., 1975. Dark inhibition of egg hatching of the marine copepod Acartia clausi Giesbracht. J. exp. mar. Biol. Ecol. 20: 43–47.Google Scholar
  35. Lindley, J. A., 1986. Dormant eggs of calanoid copepods in sea-bed sediments of the English Channel and southern North Sea. J. Plankton Res. 8: 399–400.Google Scholar
  36. Lindley, J. A., 1990. Distribution of overwintering calanoid copepod eggs in sea-bed sediments around southern Britain. Mar. Biol. 104: 209–217.Google Scholar
  37. Lindley, J. A., 1992. Resistant eggs of the Centropagoidea (Copepoda:Calanoida): a possible preadaptation to colonization of inland waters. J. Crust. Biology 12: 368–371.Google Scholar
  38. Lindley, J. A. & H. G. Hunt, 1989. The distribution of Labidocera wollastoni and Centropages hamatus in the North Atlantic Ocean and the North Sea in relation to the role of resting eggs in the sediment. In: Ryland, J. S., Tyler, P. A. (eds), Reproduction, genetics, and distributions of marine organisms. Olsen and Olsen, Fredensborg: 407–413.Google Scholar
  39. Lutz, R. V., N. H. Marcus & J. P. Chanton, 1992. Effects of low oxygen concentrations on the hatching and viability of eggs of marine calanoid copepods. Mar. Biol. 114: 241–247.Google Scholar
  40. Lutz, R. V., N. H. Marcus & J. P. Chanton, 1994. Hatching and viability of copepod eggs at two stages of embryological development: anoxic/hypoxic effect. Mar. Biol. 199–204.Google Scholar
  41. Marcus, N. H., 1980. Photoperiodic control of diapause in the marine calanoid copepod Labidocera aestiva. Biol. Bull. 159: 311–318.Google Scholar
  42. Marcus, N. H., 1982a. The reversibility of subitaneous and diapause egg production by individual females of Labidocera aestiva (Copepoda:Calanoida). Biol. Bull. 162: 39–44.Google Scholar
  43. Marcus, N. H., 1982b. Photoperiodic and temperature regulation of diapause of Labidocera aestiva (Copepoda:Calanoida). Biol. Bull. 162: 45–52.Google Scholar
  44. Marcus, N. H., 1984b. Variation in the diapause response of Labidocera aestiva (Copepoda:Calanoida) from different latitudes and its importance in the evolutionary process. Biol. Bull. 166: 127–139.Google Scholar
  45. Marcus, N. H., 1984b. Recruitment of copepod nauplii into the plankton: importance of diapause eggs and benthic processes. Mar. Ecol. Prog. Ser. 15: 47–54.Google Scholar
  46. Marcus, N. H., 1987. Differences in the duration of egg diapause of Labidocera aestiva (Copepoda:Calanoida) from the Woods Hole, Massachussetts, region. Biol. Bull. 173: 169–177.Google Scholar
  47. Marcus, N. H., 1989. Abundance in bottom sediments and hatching requirements of eggs of Centropages hamatus (Copepoda:Calanoida) from the Alligator Harbor region, Florida. Biol. Bull. 176: 142–146.Google Scholar
  48. Marcus, N. H., 1990. Calanoid copepod, cladoceran, and rotifer eggs in seabottom sediments of northern California coastal waters:identification, occurrence, and hatching. Mar. Biol. 105: 413–418.Google Scholar
  49. Marcus, N. H., 1991. Planktonic copepods in a sub-tropical estuary:seasonal patterns in the abundance of adults, copepodites, nauplii, and eggs in the sea bed. Biol. Bull. 181: 269–274.Google Scholar
  50. Marcus, N. H. In press. Population dynamics of copepods in northern California coastal waters: benthic-pelagic coupling. Mar. Biol.Google Scholar
  51. Marcus, N. H. & C. M. Fuller, 1986. Subitaneous and diapause eggs of Labidocera aestiva (Copepoda:Calanoida): differences in fall velocity and density. J. exp. mar. Biol. Ecol. 99: 247–256.Google Scholar
  52. Marcus, N. H. & C. M. Fuller, 1989. Distribution and abundance of eggs of Labidocera aestiva (Copepoda:Calanoida) in the bottom sediments of Buzzards Bay, Massachusetts USA. Mar. Biol. 100: 319–326.Google Scholar
  53. Marcus, N. H. & R. V. Lutz, 1994. Effects of anoxia on the viability of subitaneous eggs of planktonic copepods. Mar. Biol. 121: 83–87.Google Scholar
  54. Marcus, N. H., R. V. Lutz, W. Burnett & P. Cable, 1994. Age, viability, and vertical distribution of zooplankton resting eggs from an anoxic basin: Evidence of an egg bank. Limnol. Oceanogr. 39: 154–158.Google Scholar
  55. Marcus, N. H. & J. Schmidt-Gengenbach, 1986. Recruitment of individuals into the plankton: the importance of bioturbation. Limnol. Oceanogr. 31: 206–210.Google Scholar
  56. Marcus, N. H. & K. Taulbee, 1992. Potential effects of a resuspension event on the vertical distribution of copepod eggs in the sea bed: a laboratory simulation. Mar. Biol. 114: 249–251.Google Scholar
  57. McMinn, A., C. Bolch & G. Hallegraeff, 1992. Cobricosphaeridium Harland and Sarjeant: Dinoflagellate cyst or copepod egg. Micropaleontology 38: 315–316.Google Scholar
  58. Miller, D. D. & N. H. Marcus, 1994. The effects of salinity and temperature on the density and sinking velocity of eggs of the calanoid copepod Acartia tonsa Dana. J. exp. mar. Biol. Ecol. 179: 235–252.Google Scholar
  59. Naess, T., 1991a. Marine calanoid resting eggs in Norway: abundance and distribution of two copepod species in the sediment of an enclosed basin. Mar. Biol. 110: 261–266.Google Scholar
  60. Naess, T., 1991b. Tolerance of marine calanoid resting eggs: effects of freezing, dessication and Rotenone exposure-afield and laboratory study. Mar. Biol. 111: 455–459.Google Scholar
  61. Pertzova, N. M., 1974. Life cycle and ecology of a thermophilous copepod Centropages hamatus in the White Sea. Zool. Zh. 53: 1013–1022 (in Russian).Google Scholar
  62. Sazhina, L. I., 1968. On hibernating eggs of marine Calanoida. Zool. Zh. 47: 1554–1556 (in Russian).Google Scholar
  63. Santella, L. & A. Ianora, 1990. Subitaneous and diapause eggs in Mediterranean populations of Pontella mediterranea (Copepoda:Calanoida): a morphological study. Mar. Biol. 105: 83–90.Google Scholar
  64. Santella, L. & A. Ianora, 1992. Fertilization envelope in diapause eggs of Pontella mediterranea (Crustacean, Copepoda). Molecular Reproduction and Development 33: 463–469.Google Scholar
  65. Sullivan, B. K. & L. T. McManus, 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: 121–128.Google Scholar
  66. Tauber, C. & M. Tauber, 1981. Insect seasonal life cycles: Genetics and Evolution. Annu. Rev.Ecol. Syst. 12: 281–308.Google Scholar
  67. Uye, S., 1980. Development of neretic copepods Acartia clausi and A. steuri. I. Some environmental factors affecting egg development and the nature of resting eggs. Bull. Plank. Soc. Japan 27: 1–9.Google Scholar
  68. Uye, S., 1985. Resting egg production as a life history strategy of marine planktonic copepods. Bull. Mar. Sci. 37: 440–449.Google Scholar
  69. Uye, S. & A. Fleminger, 1976. Effect of various environmental factors on egg development of several species of Acartia in Southern California. Mar. Biol. 38: 253–262.Google Scholar
  70. Uye, S., S. Kasahara & T. Onbe, 1979. Calanoid copepod eggs in sea-bottom muds. IV. Effects of some environmental factors on the hatching of resting eggs. Mar. Biol. 51: 151–156.Google Scholar
  71. Uye, S., M. Yoshiya, K. Ueda & S. Kasahara, 1985. The effect of organic seabottom pollution on survivability of resting eggs of neretic calanoids. Crustaceana 46: 390–405.Google Scholar
  72. Viitasalo, M., 1992. Calanoid resting eggs in the Baltic Sea: implications for the population dynamics of Acartia bifilosa (Copepoda). Mar. Biol. 114: 397–405.Google Scholar
  73. Zhong, X-F. & Y.-C. Xiao, 1992. Resting eggs of Acartia bifilosa Giesbrecht and A. pacifica Steuer in Jiaozhou Bay. Marine Sciences (Qingdao). No. 5: 55–59. (In Chinese with English summary).Google Scholar
  74. Zillioux, E. J. & J. G. Gonzalez, 1972. Egg dormancy in a neritic calanoid copepod and its implications to overwintering in boreal waters. In, B. Battaglia (ed.), Fifth European marine biology Symposium. Piccin Editore, Padova: 217–230.Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • Nancy H. Marcus
    • 1
  1. 1.Department of OceanographyFlorida State UniversityTallahasseeUSA

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