Bio-foam enhances larval retention in a free-spawning marine tunicate

Abstract

Here we report a mechanism that reduces dispersal of early developing stages and larvae in a free-spawning intertidal and shallow subtidal tunicate, Pyura praeputialis (Heller 1878), in the Bay of Antofagasta, Chile. The spawning of gametes by the tunicate into the naturally turbulent aerated seawater decreases their surface tension and induces the formation of a bio-foam. Water collected from foamy intertidal pools and tide channels showed a high concentration of P. praeputialis early developing stages and tadpole larvae in the foam. Because gametes are synchronically spawned for external fertilization and larvae settle near adults, our results suggest that this bio-foam increases fertilization success and effective settlement of their short-lived larvae in the vicinity of the adults spawning the gametes. This mechanism reinforces published evidence suggesting that local retention of intertidal and inshore marine invertebrate larvae may be more common than previously thought, offering, for instance, new perspectives for the design and networking of marine protected and management areas.Chile ͉ surface tension ͉ tide channels ͉ broadcast spawner ͉ settlement I t is well known that surfactants can induce the formation of bio-foams that can ensure egg retention and larval development in organisms such as tropical leptodactylid frogs (1-5) and African and Asian freshwater labyrinth fishes (6). However, such egg-larval retentive mechanisms or ''foam-nests'' have not been reported for marine organisms. In Chile, massive populations of the intertidal and shallow subtidal tunicate Pyura praeputialis form beds almost exclusively along a 60-70 km stretch of the rocky shoreline inside the Bay of Antofagasta (7). This tunicate is an alien species in Chile, and its absence at locations more than 3-5 km outside of the Bay of Antofagasta, and along the Chilean coast, suggests the existence of unknown mechanisms preventing its dispersal (8) and maintaining high settlement inside the Antofagasta tunicate beds. In December 2004 and January 2005, midway through the ebb tides, we observed massive co-spawning of both eggs and sperm suspension from P. praeputialis into naturally turbulent aerated intertidal seawater (Fig. 1A) and the subsequent formation of localized and conspicuous masses of foams. These bio-foam masses persisted for several hours on top of rocky shores and floating in tidal channels, near where they were spawned, because of onshore winds (Fig. 1). Results and DiscussionTo investigate the role of the bio-foam associated with P. praeputialis on the retention of embryos and tadpole larvae of the species, seawater samples were collected (December 10 and 12, 2004; January 14 and 15, 2005) by using a plankton bilgepump equipped with a 50-m elbow end and calibrated with a domestic flow meter (9). The pump was used to collect water samples at different time intervals through the tide cycle from the sea surface just above or near the intertidal rocky shores in Bay of Antofagasta that are dominated by P. praeputialis. Eac...

Gamete plasticity in a broadcast spawning marine invertebrate

“…This may in turn have wider implications for postsettlement survival of offspring. Some ascidians spawn in conditions that promote gamete and larval retention (58)(59)(60) and are therefore unlikely to disperse far from their natal habitat. This means that in addition to being a good predictor of the sperm environment, local density may also be a good predictor of offspring environment.…”

Biological modification of mechanical properties of the sea surface microlayer, influencing waves, ripples, foam and air-sea fluxes

“…For instance, both freshwater and marine foams have been found to efficiently trap particulate organic matter, such as fungal spores (Kohlmeyer, 1984) that can be stored in foams in a viable, ungerminated state for considerable periods of time (Harrington, 1997;Pascoal et al, 2005), dense populations of bacteria, algae and protozoa (Maynard, 1968;Tsyban, 1971;Schlichting, 1974;Velimirov, 1980;Eberlein et al, 1985;Napolitano and Richmond, 1995), and metazoa such as insects, polychaetes, mussels and crustaceans (Castilla et al, 2007). Foams have also been suggested to act as a source of nutrients (Harner et al, 2004) for pelagic and intertidal organisms (Bärlocher et al, 1988;Craig et al, 1989) due to their high calorific content (Velimirov, 1980).…”

Biofoams and natural protein surfactants

“…One exception is the recently described foam accumulations associated with the synchronous reproductive stages of a species of marine tunicate (sea squirt) that appears to enhance fertilization of eggs and assist in the settling and retention of the larvae during spawning [20]. These foams are found on rocky beaches and tidal channels in inter-tidal regions in Chile, where tunicate eggs and larvae would otherwise be dispersed by wave activity.…”