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A Laboratory Study of the Effect of Temperature on the Embryonic Diapause of the Hermit Crab Pagurus proximus Komai, 2000 (Decapoda: Paguridae) from Peter the Great Bay, Sea of Japan

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Abstract

Under laboratory conditions, the effect of temperature on the reversible arrest in embryo development, which occurs as a result of winter spawning, was studied in the hermit crab Pagurus proximus, Komai, 2000 from Amurskiy Bay (Peter the Great Bay, Sea of Japan). In clutches of females that spawned under natural conditions at a water temperature of 5°C and below, an increase in water temperature to 14–16°C led to the termination of embryonic diapause and the synchronous resumption of egg development, regardless of whether the temperature conditions changed at the beginning or at the end of the winter breeding season. No embryonic diapause was observed in clutches of females of P. proximus that were captured in December–April and spawned in the laboratory at a water temperature of 14–16°С. From this it follows that the primary signal for diapause initiation and termination in P. proximus is temperature, which directly affects the embryo. The data we obtained confirm that embryonic diapause of the hermit crab P. proximus is not obligate but is induced by habitat conditions, primarily by ambient temperature. The possibility of using P. proximus as a model object for studying the mechanisms of embryonic diapause in decapods is considered.

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REFERENCES

  1. Alekseev, V.R., Physiological and molecular biological mechanisms underlying diapause in aquatic invertebrates, Russ. J. Dev. Biol., 2010, vol. 41, no. 2, pp. 61–70.

    Article  CAS  Google Scholar 

  2. Kornienko, E.S., The reproductive strategy of hermit crabs in temperate waters, Russ. J. Mar. Biol., 2020, vol. 46, no. 5, pp. 319–329.

    Article  Google Scholar 

  3. Kornienko, E.S. and Korn, O.M., A key for the identification of the zoeae of common species of hermit crabs (Decapoda: Paguroidea) of Vostok Bay, the Sea of Japan, Russ. J. Mar. Biol., 2016, vol. 42, no. 5, pp. 419–426.

    Article  Google Scholar 

  4. Kornienko, E.S. and Selin, N.I., The population and reproductive characteristics of the hermit crab Pagurus brachiomastus (Thallwitz, 1892) (Decapoda: Paguridae) from Peter the Great Bay, the Sea of Japan, Russ. J. Mar. Biol., 2019, vol. 45, no. 3, pp. 174–184. https://doi.org/10.1134/S1063074019030088

    Article  Google Scholar 

  5. Lotsiya severo-zapadnogo berega Yaponskogo morya ot reki Tumannaya do mysa Belkina (Sailing Directions for the Northwestern Shore of the Sea of Japan: From the Tumannaya River to Cape Belkin), Moscow: Gl. Upr. Navig. Okeanogr., 1984.

  6. Luchin, V.A., Tikhomirova, E.A., and Kruts, A.A., Oceanographic regime of Peter the Great Bay (Sea of Japan), Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2005, vol. 140, pp. 130–169.

    Google Scholar 

  7. Selin, N.I., Kornienko, E.S., and Korn, O.M., The species composition and pattern of distribution of hermit crabs (Decapoda: Paguroidea) in Vostok Bay, Sea of Japan, Russ. J. Mar. Biol., 2016, vol. 42, no. 6, pp. 481–488.

    Article  Google Scholar 

  8. Alekseev, V.R., Hwang, J.-S., and Tseng, M.-H., Diapause in aquatic invertebrates: what’s known and what’s next in research and medical application?, J. Mar. Sci. Technol., 2006, vol. 14, no. 4, art. ID 9.

    Article  Google Scholar 

  9. Alekseev, V.R. and Starobogatov, Y.I., Types of diapause in Crustacea: definitions, distribution, evolution, Hydrobiologia, 1996, vol. 320, pp. 15–26.

    Article  Google Scholar 

  10. Alekseev, V.R. and Vinogradova, E.B., Introduction to dormancy in aquatic invertebrates: mechanism of induction and termination, hormonal and molecular-genetic basis, in Dormancy in Aquatic Organisms: Theory, Human Use and Modeling, vol. 92: Monographiae Biologicae, Cham: Springer-Verlag, 2019, pp. 7–41.

  11. Anger, K., The Biology of Decapod Crustacean Larvae, vol. 14: Crustacean Issues, Lisse: A.A. Balkema, 2001.

    Google Scholar 

  12. Baumgartner, M.F. and Tarrant, A.M., The physiology and ecology of diapause in marine copepods, Annu. Rev. Mar. Sci., 2017, vol. 9, pp. 387–411.

    Article  Google Scholar 

  13. Contreras-Garduño, J. and Córdoba-Aguilar, A., Sexual selection in hermit crabs: a review and outlines of future research, J. Zool., 2006, vol. 270, no. 4, pp. 595–605.

    Article  Google Scholar 

  14. Duguid, W.D.P. and Page, L.R., Biennial reproduction with embryonic diapause in Lopholithodes foraminatus (Anomura: Lithodidae) from British Columbia waters, Invertebr. Biol., 2011, vol. 130, no. 1, pp. 68–82.

    Article  Google Scholar 

  15. Fenelon, J.C., Banerjee, A., and Murphy, B.D., Embryonic diapause: development on hold, Int. J. Dev. Biol., 2014, vol. 58, nos. 2–4, pp. 163–174.

    Article  Google Scholar 

  16. Goshima, S., Kawashima, T., and Wada, S., Mate choice by males of the hermit crab Pagurus filholi: Do males assess ripeness and/or fecundity of females?, Ecol. Res., 1998, vol. 13, pp. 151–161.

    Article  Google Scholar 

  17. Goshima, S., Wada, S., and Ohmori, H., Reproductive biology of the hermit crab Pagurus nigrofascia (Anomura: Paguridae), Crustacean Res., 1996, vol. 25, pp. 86–92.

    Article  Google Scholar 

  18. Gyllström, M. and Hansson, L.A., Dormancy in freshwater zooplankton: Induction, termination and the importance of benthic-pelagic coupling, Aquat. Sci., 2004, vol. 66, pp. 274–295.

    Article  Google Scholar 

  19. Hand, S.C., Metabolic Dormancy in Aquatic Invertebrates, vol. 8: Advances in Comparative and Environmental Physiology, New York: Springer-Verlag, 1991, pp. 1–50.

    Google Scholar 

  20. Hand, S.C., Denlinger, D.L., Podrabsky, J.E., and Roy, R., Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2016, vol. 310, no. 11, pp. R1193–R1211.

    Google Scholar 

  21. Hansen, B.W., Copepod embryonic dormancy: “An egg is not just an egg”, Biol. Bull., 2019, vol. 237, no. 2, pp. 145–169.

    Article  CAS  Google Scholar 

  22. Jensen, G.C. and Armstrong, D.A., Biennial reproductive cycle of blue king crab, Paralithodes platypus, at the Pribilof Islands, Alaska, and comparison to a congener, P. camtschatica, Can. J. Fish. Aquat. Sci., 1989, vol. 46, pp. 932–940.

    Article  Google Scholar 

  23. Komai, T., Saito, Y., and Myorin, E., A new species of the hermit crab genus Pagurus Fabricius, 1775 (Crustacea: Decapoda: Anomura: Paguridae) from shallow coastal waters in Japan, with a checklist of the East Asian species of the genus, Zootaxa, 2015, vol. 3918, no. 2, pp. 224–238.

    Article  Google Scholar 

  24. Korn, O.M., Kornienko, E.S., and Selin, N.I., Population biology and reproductive characteristics of the hermit crab Pagurus minutus Hess, 1865 (Decapoda: Anomura: Paguridae) in the northern part of the species range (Peter the Great Bay, the Sea of Japan), Mar. Biol. Res., 2018, vol. 14, no. 8, pp. 846–855.

    Article  Google Scholar 

  25. Kornienko, E.S., Selin, N.I., and Korn, O.M., Population and reproductive characteristics of the hermit crab Pagurus proximus Komai, 2000 (Decapoda: Anomura: Paguridae) in the northern part of the species range, J. Mar. Biol. Assoc. U. K., 2019, vol. 99, no. 1, pp. 101–109.

    Article  Google Scholar 

  26. Lovrich, G.A. and Vinuesa, J.H., Reproductive biology of the false southern king crab (Paralomis granulosa, Lithodidae) in the Beagle Channel, Argentina, Fish. Bull., 1993, vol. 91, pp. 664–675.

    Google Scholar 

  27. Mishima, S. and Henmi, Y., Reproduction and embryonic diapause in the hermit crab Pagurus nigrofascia, Crustacean Res., 2008, vol. 37, pp. 26–34.

    Article  Google Scholar 

  28. Mishima S., Kobayashi S., Yamada K., Henmi Y. The effects of photoperiod and temperature on embryonic diapause termination in the hermit crab Pagurus nigrofascia, Plankton Benthos Res., 2021, vol. 16, no. 2, pp. 79–83.

    Article  Google Scholar 

  29. Moriyasu, M. and Lanteigne, C., Embryo development and reproductive cycle in the snow crab, Chionoecetes opilio (Crustacea: Majidae), in the southern Gulf of St. Lawrence, Canada, Can. J. Zool., 1998, vol. 76, no. 11, pp. 2040–2048.

    Article  Google Scholar 

  30. Mura, M., Orrù, F., and Cau, A., Reproduction strategy of the deep-sea hermit crabs Pagurus alatus and Pagurus excavatus of the Central-Western Mediterranean Sea, Hydrobiologia, 2006, vol. 557, pp. 51–57.

    Article  Google Scholar 

  31. Nambu, Z., Tanaka, S., and Nambu, F., Influence of photoperiod and temperature on reproductive mode in the Brine shrimp, Artemia franciscana, J. Exp. Zool., Part A., 2004, vol. 301A, pp. 542–546.

    Article  Google Scholar 

  32. Petersen, S., The embryonic development of Hyas araneus L. (Decapoda, Majidae): Effects of temperature, Sarsia, 1995, vol. 80, no. 3, pp. 193–198.

    Article  Google Scholar 

  33. Podrabsky, J.E. and Hand, S.C., Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish, J. Exp. Biol., 2015, vol. 218, no. 12, pp. 1897–1906.

    Article  Google Scholar 

  34. Reid, W.D.K., Watts, J., Clarke S., et al., Egg development, hatching rhythm and moult patterns in Paralomis spinosissima (Decapoda: Anomura: Paguroidea: Lithodidae) from South Georgia waters (Southern Ocean), Polar Biol., 2007, vol. 30, pp. 1213–1218.

    Article  Google Scholar 

  35. Stevens, B.G., Swiney, K.M., and Buck, L., Thermal effects on embryonic development and hatching for blue king crab Paralithodes platypus (Brandt, 1850) held in the laboratory, and a method for predicting dates of hatching, J. Shellfish Res., 2008, vol. 27, no. 5, pp. 1255–1263.

    Article  Google Scholar 

  36. Swiney, K.M., Egg extrusion, embryo development, timing and duration of eclosion, and incubation period of primiparous and multiparous tanner crabs (Chionoecetes bairdi), J. Crustacean Biol., 2008, vol. 28, no. 2, pp. 334–341.

    Article  Google Scholar 

  37. Turra, A. and Leite, F.P.P., Embryonic development and duration of incubation period of tropical intertidal hermit crabs (Decapoda, Anomura), Rev. Bras. Zool., 2007, vol. 24, no. 3, pp. 677–686.

    Article  Google Scholar 

  38. Wada, S. and Mima, A., Reproductive characters of the hermit crab Pagurus proximus Komai, 2000 in Hakodate Bay, southern Hokkaido, Japan, Crustacean Res., 2003, no. 32, pp. 73–78.

  39. Wada, S., Oba, T., Nakata, K., and Ito, A., Factors affecting the interval between clutches in the hermit crab Pagurus nigrivittatus, Mar. Biol., 2008, vol. 154, no. 3, pp. 501–507.

    Article  Google Scholar 

  40. Wada, S., Tanaka, K., and Goshima, S., Precopulatory mate guarding in the hermit crab Pagurus middendorffii (Brandt) (Decapoda: Paguridae): effects of population parameters on male guarding duration, J. Exp. Mar. Biol. Ecol., 1999, vol. 239, no. 2, pp. 289–298.

    Article  Google Scholar 

  41. Wang, Z., Asem, A., Okazaki, R.K., and Sun, S., The critical stage for inducing oviparity and embryonic diapause in parthenogenetic Artemia (Crustacea: Anostraca): an experimental study, J. Oceanol. Limnol., 2019, vol. 37, no. 5, pp. 1669–1677.

    Article  CAS  Google Scholar 

  42. Wear, R.G., Incubation in British decapod Crustacea, and the effects of temperature on the rate and success of embryonic development, J. Mar. Biol. Assoc. U. K., 1974, vol. 54, no. 3, pp. 745–762.

    Article  Google Scholar 

  43. Webb, J.B., Eckert, G.L., Shirley, T.C., and Tamone, S.L., Changes in embryonic development and hatching in Chionoecetes opilio (snow crab) with variation in incubation temperature, Biol. Bull., 2007, vol. 213, no. 1, pp. 67–75.

    Article  Google Scholar 

  44. Zadereev, E. and Lopatina, T.S., The role of chemical interactions in embryonic diapause induction in zooplankton, in Dormancy in Aquatic Organisms, Theory, Human Use and Modeling, vol. 92: Monographiae Biologicae, Cham: Springer-Verlag, 2019, pp. 175–186.

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ACKNOWLEDGMENTS

The author is grateful to the team of the Diving Department of the National Scientific Center of Marine Biology of the FEB RAS, who captured hermit crabs under difficult winter conditions, as well as to the staff of the Aquarium Department for long-term maintenance of the animals.

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  1. Zhirmunsky National Scientific Center of Marine Biology, Far East Branch, Russian Academy of Sciences, 690041, Vladivostok, Russia

    E. S. Kornienko

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Translated by T. Koznova

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Kornienko, E.S. A Laboratory Study of the Effect of Temperature on the Embryonic Diapause of the Hermit Crab Pagurus proximus Komai, 2000 (Decapoda: Paguridae) from Peter the Great Bay, Sea of Japan. Russ J Mar Biol 48, 231–237 (2022). https://doi.org/10.1134/S1063074022040058

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