Abstract
Grading procedure in routine sea cucumber hatchery production is thought to affect juvenile sea cucumber immunological response. The present study investigated the impact of a 3-min mechanical perturbation mimicking the grading procedure on neuroendocrine and immune parameters of the sea cucumber Apostichopus japonicus. During the application of stress, concentrations of noradrenaline and dopamine in coelomic fluid increased significantly, indicating that the mechanical perturbation resulted in a transient state of stress in sea cucumbers. Coelomocytes concentration in coelomic fluid increased transiently after the beginning of stressing, and reached the maximum in 1 h. Whereas, coelomocytes phagocytosis at 3 min, superoxide anion production from 3 min to 0.5 h, acid phosphatase activity at 0.5 h, and phenoloxidase activity from 3 min to 0.5 h were all significantly down-regulated. All of the immune parameters recovered to baseline levels after the experiment was conducted for 8 h, and an immunostimulation occurred after the stress considering the phagocytosis and acid phosphatase activity. The results suggested that, as in other marine invertebrates, neuroendocrine/immune connections exist in sea cucumber A. japonicus. Mechanical stress can elicit a profound influence on sea cucumber neuroendocrine system. Neuroendocrine messengers act in turn to modulate the immunity functions. Therefore, these effects should be considered for developing better husbandry procedures.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Adamo, S. A., 2012. The effects of the stress response on immune function in invertebrates: An evolutionary perspective on an ancient connection. Hormones and Behavior, 62: 324–330.
Aladaileh, S., Mohammad, M. G., Ferrari, B., Nair, S. V., and Raftos, D. A., 2008. In vitro effects of noradrenaline on the Sydney rock oyster (Saccostrea glomerata). Comparative Biochemistry and Physiology Part A, 151: 691–697.
Ballarin, L., Pampanin, D. M., and Marin, M. G., 2003. Mechanical disturbance affects haemocyte functionality in the venus clam Chamelea gallina. Comparative Biochemistry and Physiology Part A, 136: 631–640.
Bayne, B. L., 1990. Phagocytosis and non-self recognition in invertebrates. Phagocytosis appears to be an ancient line of defense. Bioscience, 40: 723–731.
Bussell, J. A., Gidman, E. A., Causton, D. R., Gwynn-Jones, D., Malham, S. K., Jones, M. L., Reynolds, B., and Seed, R., 2008. Changes in the immune response and metabolic fingerprint of the mussel, Mytilus edulis (Linnaeus) in response to lowered salinity and physical stress. Journal of Experimental Marine Biology and Ecology, 358: 78–85.
Chang, C. C., Hung, M. D., and Cheng, W., 2011. Norepinephrine depresses the immunity and disease-resistance ability via α1- and β1-adrenergic reciptors of Macrobrachium rosenbergii. Developmental and Comparative Immunology, 35: 685–691.
Chang, C. C., Yeh, M. S., and Cheng, W., 2009. Cold shock-induced norepinephrine triggers apoptosis of haemocytes via caspase-3 in the white shrimp Litopenaeus vannamei. Fish & Shellfish Immunology, 27: 695–700.
Cheng, W., Chieu, H. T., Ho, M. C., and Chen, J. C., 2006. Noradrenaline modulates the immunity of white shrimp Litopenaeus vannamei. Fish & Shellfish Immunology, 21: 11–19.
Cheng, W., Hsiao, I. S., Hsu, C. H., and Chen, J. C., 2004. Change in water temperature on the immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Fish & Shellfish Immunology, 17: 235–243.
Chrousos, G. P., and Gold, P. W., 1992. The concepts of stress and stress system disorders. Overview of physical and behavioural homeostasis. Journal of the American Medical Association, 267: 1244–1252.
Chu, F. L. E., and Hale, R. C., 1994. Relationship between pollution and susceptibility to infectious disease in the eastern oyster, Crassostrea virginica. Marine Environmental Research, 38: 243–256.
Coteur, G., Corriere, N., and Dubois, P. H., 2004. Environmental factors influencing the immune response of the common European starfish (Asterias rubens). Fish & Shellfish Immunology, 16: 51–63.
Department of Fisheries (DOF), 2014. China Fisheries Statistic Yearbook 2014. China Agriculture Press, Beijing, 64pp (in Chinese).
Dolmatova, L. S., Eliseykina, M. G., Timchenko, N. F., Kovaleva, A. L., and Shitkova, O. A., 2003. Generation of reactive oxygen species in different fractions of the coelomocytes of holothurian Eupentacta fraudatrix in response to the thermostable toxin of Yersinia pseudotuberculosis in vitro. Chinese Journal of Ocean and Limnology, 21: 293–304.
Dong, S., Liang, M., Gao, Q., Wang, F., Dong, Y., and Tian, X., 2010. Intra-specific effects of sea cucumber (Apostichopus japonicus) with reference to stocking density and body size. Aquaculture Research, 41: 1170–1178.
Gu, M., Ma, H. M., Mai, K. S., Zhang, W. B., Ai, Q. H., Wang, X. J., and Bai, N., 2010. Immune response of sea cucumber Apostichopus japonicus coelomocytes to several immunostimulants in vitro. Aquaculture, 306: 49–56.
Holm, K., Dupont, S., Skold, H., Stenius, A., Thorndyke, M., and Hernroth, B., 2008. Induced cell proliferation in putative haematopoietic tissues of the sea star, Asterias rubens (L.). Journal of Experimental Biology, 211: 2551–2558.
Hooper, C., Day, R., Slocombe, R., Benkendorff, K., and Handlinger, J., 2011. Effect of movement stress on immune function in farmed Australian abalone (hybrid Haliotis laevigata and Haliotis rubra). Aquaculture, 315: 348–354.
Husmann, G., Philipp, E. E. R., Rosenstiel, P., Vazquez, S., and Abele, D., 2011. Immune response of the Antarctic bivalve Laternula elliptica to physical stress and microbial exposure. Journal of Experimental Marine Biology and Ecology, 398: 83–90.
Klanian, M. G., 2013. Physiological and immunological conditions of the sea cucumber Isostichopus badionotus (Selenka, 1867) during dormancy. Journal of Experimental Marine Biology and Ecology, 444: 31–37.
Kuchel, R. P., McCarthy, A., and Raftos, D. A., 2012. Phenoloxidase activity as an indicator of stress in the silver-lip pearl oyster, Pinctada maxima. Aquaculture, 364–365: 224–229.
Kuchel, R. P., Raftos, D. A., and Nair, S., 2010. Immunosuppressive effects of environmental stressors on immunological function in Pinctada imbricata. Fish & Shellfish Immunology, 29: 930–936.
Lacoste, A., Jalabert, F., Malham, S. K., Cueff, A., and Poulet, S. A., 2001a. Stress and stress-induced neuroendocrine changes increase the susceptibility of juvenile oysters (Crassostrea gigas) to Vibrio splendidus. Applied and Environmental Microbiology, 67: 2304–2309.
Lacoste, A., Malham, S. K., Cueff, A., Jalabert, F., Gelebart, F., and Poulet, S. A., 2001b. Evidence for a form of adrenergic response to stress in the mollusk Crassostrea gigas. The Journal of Experimental Biology, 204: 1247–1255.
Lacoste, A., Malham, S. K., Cueff, A., and Poulet, S. A., 2001c. Noradrenaline modulates hemocyte reactive oxygen species production via β-adrenergic receptors in the oyster Crassostrea gigas. Developmental and Comparative Immunology, 25: 285–289.
Lacoste, A., Malham, S. K., Cueff, A., and Poulet, S. A., 2001d. Noradrenaline inhibits phagocytosis by hemocytes of the oyster Crassostrea gigas via a β-adrenoceptor/cAMP signaling pathway. General and Comparative Endocrinology, 122: 252–259.
Lacoste, A., Malham, S. K., Cueff, A., and Poulet, S. A., 2001e. Noradrenaline reduces the stimulatory effect of interleukin-1 alpha on reactive oxygen species production by oyster immunocytes. Invertebrate Biology, 120: 358–364.
Lacoste, A., Malham, S. K., Gelebart, F., Cueff, A., and Poulet, S. A., 2002. Stress-induced immune changes in the oyster Crassostrea gigas. Developmental and Comparative Immunology, 26: 1–9.
Liu, C. H., and Chen, J. C., 2004. Effect of ammonia on the immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus. Fish & Shellfish Immunology, 16: 321–334.
Liu, Z. M., Ma, Y. X., Yang, Z. P., Li, M., Liu, J., and Bao, P. Y., 2012. Immune responses and disease resistance of the juvenile sea cucumber Apostichopus japonicus induced by Me-tschnikowia sp. C14. Aquaculture, 368–369: 10–18.
Malham, S. K., Lacoste, A., Gelebart, F., Cueff, A., and Poulet, S. A., 2002. A first insight into stress-induced neuroendocrine and immune changes in the octopus Eledone cirrhosa. Aquatic Living Resources, 15: 187–192.
Malham, S. K., Lacoste, A., Gelebart, F., Cueff, A., and Poulet, S. A., 2003. Evidence for a direct link between stress and immunity in the mollusc Haliotis tuberculata. Journal of Experimental Zoology Part A, 295: 136–144.
Ottaviani, E., and Franceschi, C., 1996. The neuroendocrinology of stress from invertebrates to man. Progress in Neurobiology, 48: 421–440.
Pampanin, D. M., Ballarin, L., Carotenuto, L., and Marin, M. G., 2002. Air exposure and functionality of Chamelea gallina haemocytes: Effects on haematocrit, adhesion, phagocytosis and enzyme contents. Comparative Biochemistry and Physiology Part A. 131: 605–614.
Pan, L., Hu, F., and Zheng, D., 2011. Effect of dopamine injection on the hemocyte count and prophenoloxidase system of the white shrimp Litopenaeus vannamei. Journal of Ocean University of China, 10: 280–286.
Pequeux, A., Le Bras, P., Cann-Moisan, C., Caroff, J., and Seberet, P., 2002. Polyamines, indolamines, and catecholamines in gills and haemolymph of the euryhaline crab, Eriocheir sinensis, effects of high pressure and salinity. Crustaceana, 75: 567–578.
Qu, Y., Li, X., Yu, Y., Vandepeer, M., Babidge, P., Clarke, S., Bott, K., and Li, H., 2009. The effect of different grading equipment on stress levels assessd by catecholamine measurements in Pacific oysters, Crassostrea gigas (Thunberg). Aquacultural Engineering, 40: 11–16.
Roch, P., 1999. Defense mechanisms and disease prevention in farmed marine invertebrates. Aquaculture, 172: 125–145.
Schmid-Hempel, P., 2003. Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London Series B, 270: 375–466.
Simon, B. A., Pinon, M., Racotta, R., and Racotta, I. S., 2010. Neuroendocrine and metabolic responses of Pacific whiteleg shrimp Litopenaeus vannamei exposed to acute handling stress. Aquaculture, 298: 308–314.
Wang, F. Y., Yang, H. S., Gabr, H. R., and Gao, F., 2008. Immune condition of Apostichopus japonicus during aestivation. Aquaculture, 285: 238–243.
Wang, Y. J., Hu, M. H., Cheung, S. G., Shin, P. K. S., Lu, W. Q., and Li, J. L., 2012. Immune parameter changes of hemocytes in green-lipped mussel Perna viridis exposure to hypoxia and hyposalinity. Aquaculture, 356–357: 22–29.
Zhang, Q., Ma, H. M., Mai, K. S., Zhang, W. B., Liufu, Z. G., and Xu, W., 2010. Interaction of dietary Bacillus subtilis and fructooligosaccharide on the growth performance, non-specific immunity of sea cucumber, Apostichopus japonicus. Fish & Shellfish Immunology, 29: 204–211.
Zhao, Y. C., Ma, H. M., Zhang, W. B., Ai, Q. H., Mai, K. S., Xu, W., Wang, X. J., and Liufu, Z. G., 2011. Effects of dietary β-glucan on the growth, immune responses and resistance of sea cucumber, Apostichopus japonicus against Vibrio splendidus infection. Aquaculture, 315: 269–274.
Author information
Authors and Affiliations
Corresponding author
Additional information
These authors contributed equally to this work.
Rights and permissions
About this article
Cite this article
Tan, J., Li, F., Sun, H. et al. Mechanical stress induces neuroendocrine and immune responses of sea cucumber (Apostichopus japonicus). J. Ocean Univ. China 14, 350–356 (2015). https://doi.org/10.1007/s11802-015-2435-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-015-2435-1