Evidence for a direct link between stress and immunity in the mollusc Haliotis tuberculata

Abstract

Stress is thought to cause increased disease outbreaks and mortality in a number of invertebrates but currently very little information is available on mechanisms linking physiological states of stress and reduced disease resistance in these organisms. In the present study, we examined the possibility that stress alters immune functions, the principal line of defense against pathogens, in a molluscan model, the abalone Haliotis turbeculata. Immune parameters were investigated in abalones subjected to a 15 min mechanical disturbance which, as indicated by noradrenaline and dopamine hemolymphatic levels, resulted in a transient state of physiological stress. During the application of the stressor, immune parameters such as the number of circulating hemocytes, the migratory activity, the phagocytic capacity and the respiratory burst responses of hemocytes, decreased significantly. All parameters returned to initial values within 15-30 min after the end of the disturbance and a transient period of immunostimulation occurred between 100 and 480 min after the stress for all immune parameters except intracellular superoxide anion production. These results indicate that in the abalone H. tuberculata, as in vertebrates, a link exists between stress and the immune system. This may begin to answer why stress and disease outbreaks are linked in shellfish.

Stress and immune responses in abalone: Limitations in current knowledge and investigative methods based on other models

“…Several recent studies have greatly advanced our knowledge of the effect of stress on the immune response of abalone [5][6][7][8][9][10]. Malham et al [5] demonstrated that after mechanical shaking of Haliotis tuberculata, hemolymph concentrations of the stress hormones Noradrenaline and Dopamine rise, then decrease back to basal levels.…”

“…Malham et al [5] demonstrated that after mechanical shaking of Haliotis tuberculata, hemolymph concentrations of the stress hormones Noradrenaline and Dopamine rise, then decrease back to basal levels. They reported transient immune depression followed by stimulation.…”

“…Table 1 summarises the limited research that has been undertaken to date on stress and/or immune responses in abalone. Recently, a link has been established in abalone between increased stress and decreased immune functional capacity [4][5][6][7][8][9][10], leading to increased rates of bacterial infections and increased mortality [6][7][8][9][10]. This link is based on immune function tests carried out after applying stressors such as altered salinity, shaking, decreased dissolved oxygen, increased concentrations of ammonia and nitrate and increased temperature.…”

Age-dependent expression of stress and antimicrobial genes in the hemocytes and siphon tissue of the Antarctic bivalve, Laternula elliptica, exposed to injury and starvation

“…Further, in the clam R. philippinarum (Oubella et al 1993) and the Sydney rock oyster Saccostrea glomerata, starvation reduced hemocyte numbers and decreased phenol oxidase, peroxidase, and acid phosphatase activities (Butt et al 2007). Similarly, mechanical disturbance (shaking) reduced hemocyte abundance and oxidative burst activity in abalones Haliotis tuberculata and blue mussels Mytilus edulis (Bussell et al 2008;Malham et al 2003). In contrast, increased hemocyte numbers were observed in response to shell injury in deep-sea vent mussels Bathymodiolus azoricus (Kadar 2008) and in the Antarctic clam L. elliptica (Husmann et al 2011).…”

Analysis of heat, cold or salinity stress-inducible genes in the Pacific abalone, Haliotis discus hannai, by suppression subtractive hybridization

“…Recently, a link has been established in abalone between increased stress and decreased immune functional capacity (Martello and Tjeerdema, 2001;Malham et al, 2003;Cheng et al, 2004a;2004b;2004c;2004d;2004e), leading to increased rates of bacterial infections and increased mortality (Cheng et al, 2004b;2004c;2004d;2004e). This link is based on immune function tests carried out after applying stressors such as altered salinity, shaking, decreased dissolved oxygen, increased concentrations of ammonia and nitrate and increased temperature.…”