Explorations on the ecological role of toxin secretion and delivery in jawless predatory Polychaeta

Abstract

Motivated by biotechnological prospects, there is increasing evidence that we may just be scraping the tip of the iceberg of poisonous marine invertebrates, among which the Polychaeta are promising candidates for bioprospecting. Here we show that an inconspicuous phyllodocid uses toxins in its uncanny feeding strategy. The worm, a jawless active predator characterised by its bright green colour, preys on larger invertebrates (including conspecifics) by extracting tissue portions with its powerful proboscis through suction. The animal is even able to penetrate through the valves and plates of live molluscs and barnacles. Observations in situ and a series of experiments demonstrated that the worm compensates its simple anatomy with secretion of a novel toxin, or mixture of toxins, referred to by us as “phyllotoxins”. These are carried by mucus and delivered via repeated contact with the tip of the proboscis until the prey is relaxed or immobilised (reversibly). Proteolytic action permeabilises material to toxins and softens tissue to enable extraction by suction. The findings show that toxins are a major ecological trait and therefore play a key role in evolutionary success and diversification of Polychaeta, demonstrating also that understanding adaptative features may become the best showcase for novel animal toxins.

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

“…The suction action of the proboscis and the secretion of mucins and enzymes that were only briefly addressed by Michel (), have been recently detailed by Cuevas et al. (). Despite these previous works, there is still little information on Polychaeta concerning their feeding strategies.…”

“…), these cells, especially those located in the vicinity of tentacles, are thus likely associated to toxin secretion (see Cuevas et al. ).…”

“…In fact, our previous work recorded Eulalia immobilising another Polychaeta simply by repeated contact with the tip of the fully everted proboscis, at precisely the site where the toxin‐delivery tentacles are present (Cuevas et al. ).…”

“…; Cuevas et al. ). Similarly, despite the work that has been done to describe the epidermis of Polychaeta (Bubel, ; Tzetlin et al.…”

“…An effort to conjugate a relation between phenotype (behaviour included) and ecology has recently been attempted by the authors (Cuevas et al. ). The existence of specialised serous‐like cells in the proboscis was first highlighted by Michel (, ), who hypothesised their role in digestion.…”