A morphoanatomical approach to the adaptive features of the epidermis and proboscis of a marine Polychaeta: Eulalia viridis (Phyllodocida: Phyllodocidae)

Abstract

Eulalia viridis is a marine Polychaeta of the rocky intertidal that, despite its simple anatomy, is an active predator of much larger invertebrates, from which it extracts pieces of soft tissue through suction. This uncanny feeding strategy triggered the pursuit for the morphological mechanisms that enable adaptation to its environment. The evaluation of the worm anatomy and microanatomy, combining electron and optical microscopy, revealed a series of particular adaptations in the epidermis and in the proboscis (the heavily muscled eversible pharynx). Besides its function in feeding, the proboscis is the main sensory organ, being equipped with numerous sensorial papillae holding chemoreceptors. Additionally, the proboscis possesses tentacles that become exposed when the organ is everted. These provide fast release of mucus and toxins, from mucocytes and special serous cells, respectively (the latter involving both merocrine and apocrine processes), whenever contact with a prey occurs. In its turn, the epidermis provides protection by cuticle and mucus secretion and has a sensorial function that may be associated to the worm's uncommon green pigment cells. Eulalia viridis presents a series of elegant adaptive tools to cope with its environment that are evolutionarily designed to counterbalance its relatively simple body plan.

The complexity of porphyrin-like pigments in a marine annelid sheds new light on haem metabolism in aquatic invertebrates

“…It was previously noted that Eulalia does not possess complex chromatophores and owes its bright-green colour to specialised cells distributed along the skin that store the pigments in non-fluorescent cytoplasmic granules 20 . The distribution of pigment cells in the species is similar to what would be expected for melanins, for which no evidence was found asides nerve cord and eyes 21,22 . In line with the interest in porphyrins as potential photosensitisers and their physiological role as protective pigments, the aims of this study are: i) to evaluate the diversity and distribution of the pigments along E. viridis body, ii) to infer their basic spectroscopic properties and stability and iii) to contribute to understand the pigments’ adaptative value and their main functions.…”

“…In either case, it is suggested that the pigments from E. viridis hold a dual function in protecting the animal from sunlight. Besides photoreception, green pigments can take part in other sensory function, as they are present in the mechanoreceptors in the papillae of the proboscis, and in the pigment cells of skin, the latter of which possess cilia that protrude through the cuticle, being hypothesised to have a sensory-like function 22 .…”

Light-Mediated Toxicity of Porphyrin-Like Pigments from a Marine Polychaeta

“…Considering that Eulalia is a diurnal forager of the rocky intertidal, its pigments likely have two important roles. First, they are either toxic or repellent to predators and parasites that cause rupture to the pigment cells where the pigments are “safely” stored in granules [ 19 , 20 ]. Second, they warn of excessive exposure to daylight by causing physiological stress, which can be considered a form of non-nervous sensorial arrangement.…”

“…Second, they warn of excessive exposure to daylight by causing physiological stress, which can be considered a form of non-nervous sensorial arrangement. The fact that Eulalia uses its proboscis as the main organ for sensing and preying [ 19 , 21 ] explains the natural difference between the pigmentation of the skin as a major adaptive trait. These particular features, which are probably not circumscribed to Eulalia or even to the Order Phyllodocida, show that the Polychaeta are very promising targets for the bioprospecting of photoactive tetrapyrrolic pigments.…”

“…Recently, we showed that an uncanny uniformly green Polychaeta, Eulalia viridis , an opportunistic predator of the rocky intertidal, owes its coloration to a multiplicity of endogenous porphyrin-like pigments whose abundance and distribution changes between organs [ 17 , 18 , 19 , 20 ]. These pigments, which seem to almost entirely replace common biochromes such as carotenoids and melanins, were found to be chiefly stored as granules allocated within unique specialized chromocytes [ 19 , 20 ]. The function and bio-reactivity of these pigments is not, however, fully understood.…”