Ecología química en el bentos marino de la Antártida: productos naturales y defensa química en esponjas hexactinélidas, corales blandos y ascidias coloniales

Abstract

The inhabitants of marine benthos must combat the ecological pressure caused by predation, competition and fouling through a series of mechanisms, one of which is chemical defense. This type of protection is particularly extended among sessile and/or sluggish organisms, such as sponges, soft corals or ascidians. The strategies to prevent predation are related to bad taste rather than to toxicity. Moreover, they must be considered along with nutritional quality, since the more nutritious the prey, higher quantities or more potent repellents are needed to gain protection. The production of defensive secondary metabolites is energetically expensive. For this reason, the Optimal Defense Theory (ODT) predicts that defenses must be allocated in the most valuable or more exposed structures or body-regions. In Antarctic communities, the main predators are asteroids, and defensive agents are hence expected to accumulate in superficial layers of potential prey. But dense populations of amphipods, which associate opportunistically with biosubtrata, obtaining both refuge and direct or indirect sources of nutrition, are also very influencing on these bottoms. It has been reported that chemical defenses are very common in Antarctic organisms, in accordance with our results. However, the research effort has not been the same for all the groups, and there are still many aspects to learn on the chemical ecology, like the identification of the implicated products, their mode of functioning or their localization and origin. This PhD has focused on three relevant groups of the Antarctic benthos, quite understudied: hexactinellid sponges, soft corals and colonial ascidians. Two influencing sympatric predators were selected, the sea star Odontaster validus, which is a known model predator, and for the first time, the amphipod Cheirimedon femoratus, used to perform feeding experiments for the detection of repellent chemical defenses. We designed a new protocol which provided numerous methodological profits, as well as a remarkable discriminatory potential for unpalatable activities. In a survey with 31 species of Antarctic organisms, a larger incidence of unpalatable activities was recorded towards C. femoratus than against the asteroid, especially in algae and sponges, in which amphipods may particularly influence defenses distribution for representing potential host-preys. Some organisms instead, seemed to exploit alternative defensive strategies. The ecological success of the three studied groups is probably related to the presence of chemical defenses. In hexactinellid sponges these are weak, yet compensated with a low energetic content, and derive from primary metabolites, such as steroid derivates. Some glucosphingolipids instead, could have a chemotaxonomical value as chemical markers in rossellid sponges. In soft corals, chemical protection is obtained from products originating from both, primary (wax esters) and secondary metabolism (sesquiterpenoids), which seem to cooperate in an additive way, and are likely exuded within the coral mucus in living specimens. The use of primary metabolites for defense represents an effective energy saving strategy. In colonial ascidians, defensive secondary metabolites of terpenoid and alkaloid nature with potent bioactivities predominate, and in some species these are accumulated in internal tissues. Presumably, this distribution is related to the production of chemically defended lavae. Some bioactive secondary metabolites isolated from various sources, like the meridianins, may suggest a broad evolutionary retention, or a symbiotic origin. Regarding bacterial antifouling, ascidians exhibited poor activity, while some soft corals did display inhibition. With this work we provide the identification, localization, and possible origin of several defensive agents in three relevant groups of Antarctic benthic invertebrates.

Los habitantes del bentos antártico combaten la depredación, la competencia y el recubrimiento desarrollando mecanismos como la defensa química. Ésta estrategia está particularmente extendida entre organismos sésiles y organismos de cuerpo blando. Las defensas repelentes contra depredadores han de considerarse junto con la calidad nutricional, pues las dietas muy energéticas enmascaran la repelencia. La producción de metabolitos secundarios defensivos es costosa. Por ello, la Teoría de Defensa Optimizada (ODT) prevé que han de localizarse en las regiones corporales más valiosas o expuestas. En las comunidades antárticas los principales depredadores son las estrellas de mar y se postula la concentración de defensas en áreas superficiales en las presas. Pero también influyen las poblaciones de anfípodos asociados a los biosustratos, obteniendo en ellos refugio y fuente de alimentación. Esta tesis se centra en las defensas químicas de tres grupos relevantes del bentos antártico relativamente poco estudiados: esponjas hexactinélidas, corales blandos y ascidias coloniales. Se seleccionaron dos depredadores simpátricos, la estrella Odontaster validus y, por primera vez, fue utilizado el anfípodo Cheirimedon femoratus. Diseñamos un nuevo protocolo con numerosas ventajas metodológicas además de un gran potencial discriminatorio, y observamos que en 31 especies hubo mayor repelencia hacia el anfípodo que hacia la estrella, sobretodo en algas y esponjas, que podrían representar potenciales huéspedes-presa. A partir de aquí estudiamos muestras de los tres grupos seleccionados. En hexactinélidas, las defensas químicas son más débiles y derivadas del metabolismo primario, pero compensadas con un bajo valor nutricional. Algunos glucoesfingolípidos, podrían tener valor quimiotaxonómico como marcadores de la familia Rossellidae. En corales blandos existen metabolitos de defensa primarios y secundarios operando sinérgicamente, y probablemente forman parte del mucus superficial. En ascidias coloniales, los metabolitos defensivos son secundarios y muy potentes; además, en algunas especies éstos tienden a acumularse en tejidos internos, presumiblemente para producir larvas protegidas químicamente. Las ascidias mostraron poca actividad antibacteriana, pero algunos corales exhibieron respuestas inhibitorias. Esta Tesis proporciona la estructura, distribución y posible origen de los metabolitos responsables de las actividades defensivas en tres grupos relevantes de invertebrados antárticos.