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.

Cellular, Hormonal, and Behavioral Responses of the Holothuroid Cucumaria frondosa to Environmental Stressors

“…For instance, both exposure to air and lower salinities triggered an increase in phagocytes similar to results presented by Caulier et al (2020) after injection of foreign particles and following trawl collection. Phagocyte counts also aligned with the cellular reaction reported by Hamel et al (2021) who exposed C. frondosa to the predatory sea star Solaster endeca. Phagocytes were previously described as immune cells involved in phagocytosis of pathogens and in the release of humoral agents (Beck and Habicht, 1996;Rinkevich and Müller, 1996;Xue et al, 2015), suggesting that a form of internal damage occurred in sea cucumbers exposed to the most severe stressors in the present study.…”

“…While drawing fluid across the body wall using a syringe has commonly been used (e.g., Fontaine and Lambert, 1977;Galimany et al, 2018;Hou et al, 2019), this blind technique does not guarantee that only coelomic fluid is sampled because the respiratory tree, intestine, gonad, and hydrovascular system can be accidentally punctured during the process. On the other hand, the PV has not only been shown to provide a suitable source of coelomocytes and their aggregates for quantitative assessments (Li et al, 2019;Caulier et al, 2020;Hamel et al, 2021), but it has two major advantages: (i) it ensures the collection of fluid holding uncontaminated coelomocytes and aggregates, and (ii) it standardizes the origin and volume of samples across individuals, for increased reproducibility. The whole PV was emptied into a 25 mL Falcon tube to record fluid volume.…”

Crown-of-thorns starfish in captivity experience sustained large-scale changes in gene expression

“…Coelomic cells in echinoderms and other bilaterians are involved in production and/or transport of metabolites, nutrients, and signalling and immunological factors (Shabelnikov et al, 2019). Echinoderm coelomocytes are sensitive to environmental stress and can reflect the physiological state of an individual (Branco et al, 2013; Shabelnikov et al, 2019; Hamel et al, 2021). We compared gene expression in coelomocytes of wild COTS with COTS placed in captivity and either fed or not fed over 30 days.…”

“…This astonishingly large transcriptional response can be partly attributed to the conditions of captivity leading to an abnormal state of stress (Morgan and Tromborg, 2007; Fischer and Romero, 2019) that can be harmful to organismal homeostasis (Boonstra, 2013; Basile et al, 2021; Hamel et al, 2021). The wide range of potential stressors for captive animals include the abiotic environment (sound, light, odours, temperature), restriction of movement due to confinement, changes in diet, and intra- and inter-species interactions (Morgan and Tromborg, 2007; Jandt et al, 2015).…”

“…The scale of transcriptional changes induced by being removed from their natural habitat, and transported to and maintained in captivity likely reflects substantial changes in the physiology, behaviour and health of the COTS. Changes in gene expression in other animals accurately reflects changes in their physiological and developmental in a wide range of contexts (Lv et al, 2013;Meng et al, 2013;Milan et al, 2013;Hui et al, 2014;Gleason and Burton, 2015;Oomen and Hutchings, 2017;Zhang et al, 2017;Li et al, 2019;Ma et al, 2019) This astonishingly large transcriptional response can be partly attributed to the conditions of captivity leading to an abnormal state of stress (Morgan and Tromborg, 2007;Fischer and Romero, 2019) that can be harmful to organismal homeostasis (Boonstra, 2013;Basile et al, 2021;Hamel et al, 2021). The wide range of potential stressors for captive animals include the abiotic environment (sound, light, odours, temperature), restriction of movement due to confinement, changes in diet, and intra-and inter-species interactions (Morgan and Tromborg, 2007;Jandt et al, 2015).…”