Evidence of anticipatory immune and hormonal responses to predation risk in an echinoderm

Abstract

Recent efforts have been devoted to the link between responses to non-physical stressors and immune states in animals, mostly using human and other vertebrate models. Despite evolutionary relevance, comparatively limited work on the appraisal of predation risk and aspects of cognitive ecology and ecoimmunology has been carried out in non-chordate animals. The present study explored the capacity of holothuroid echinoderms to display an immune response to both reactive and anticipatory predatory stressors. Experimental trials and a mix of behavioural, cellular and hormonal markers were used, with a focus on coelomocytes (analogues of mammalian leukocytes), which are the main components of the echinoderm innate immunity. Findings suggest that holothuroids can not only appraise threatening cues (i.e. scent of a predator or alarm signals from injured conspecifics) but prepare themselves immunologically, presumably to cope more efficiently with potential future injuries. The responses share features with recently defined central emotional states and wane after prolonged stress in a manner akin to habituation, which are traits that have rarely been shown in non-vertebrates, and never in echinoderms. Because echinoderms sit alongside chordates in the deuterostome clade, such findings offer unique insights into the adaptive value and evolution of stress responses in animals.

Figure 1

Immune and behavioural responses of Cucumaria frondosa to various treatments, including no stimulus (control), direct contact with the predator (contact), chemical signature of the predator (contactless), and chemical signature of injured conspecific (injured consp.). (a) Density of coelomocytes in the Polian vesicle and (b) corresponding behavioural score over 72-h exposure. Panels (c) and (d) illustrate the same metrics integrated over the duration of the experiment (72 h) for each treatment. Values in (a) and (b) are presented as mean ± S.E. (n = 3–9) and values in (c) and (d) are presented as mean ± 95% CI (n = 15–45).

Figure 2

Immune response of Cucumaria frondosa to contactless exposure to the chemical signature of a predator over 180 min (3 h). Coelomocyte density was measured in the hydrovascular fluid of the Polian vesicle. (a) Global density of free coelomocytes (all types pooled). (b) Density of phagocytes. (c) Density of morula cells. (d) Density of hemocytes. Data presented as mean ± S.E. (n = 3). Note the different y-axis scale in (c).

Figure 3

Hormonal response of Cucumaria frondosa to contactless exposure to the chemical signature of a predator over 180 min (3 h). Cortisol concentration in pg ml⁻¹ (mean ± SE; n = 2–6) was measured in the hydrovascular fluid of the Polian vesicle.