Chemical Defense Against Fouling in the Solitary
Ascidian Phallusia nigra
BOAZ MAYZEL*, MARKUS HABER, AND MICHA ILAN
Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University,
Tel Aviv 6997801, Israel
Abstract. The solitary ascidian Phallusia nigra is rarely
fouled by epibionts. Here, we tested the antifouling activity
of its crude extracts in laboratory and field assays. P. nigra
extracts inhibited the growth of all eight tested environmen-
tal bacteria and two of four laboratory bacteria. Extracts of
the sympatric, but fouled solitary ascidian Herdmania mo-
mus inhibited only one test bacterium. Scanning electron
microscopy confirmed that the tunic surface of P. nigra is
largely bacteria-free. Both ascidian extracts significantly
inhibited the larval metamorphosis of the bryozoan Bugula
neritina at the tested concentration range of 0.05–2 mg
ml
-1
. Both crude extracts were toxic to larvae of the brine
shrimp Artemia salina at natural volumetric whole-tissue
concentrations, but only P. nigra showed activity at 2 mg
ml
-1
and below (LC
50
= 1.11 mg ml
-1
). P. nigra crude
extracts also significantly reduced the settlement of barna-
cles, polychaetes, and algae in Mediterranean field assays
and barnacle settlement in Red Sea trials. Comparisons
between control experiments and pH values monitored in all
experiments indicate that the observed effects were not due
to acidity of the organic extracts. Our results show that P.
nigra secondary metabolites have antifouling activities,
which may act in synergy with previously proposed physi-
ological antifouling mechanisms.
Introduction
In marine benthic environments, any exposed, unde-
fended, long-lived surface becomes fouled (Wahl, 1989).
The fouling process consists of multiple steps starting with
the development of an organic film by adhesion of macro-
molecules, followed by the settlement of microorganisms
and the development of a microbial biofilm. The settlement
of unicellular and multicellular eukaryotes establishes the
mature fouling community composed of prokaryotes, fungi,
diatoms, algae, protists, and invertebrates (Krug, 2006).
Fouling also occurs on the surfaces of living organisms, and
sessile marine invertebrates are particularly susceptible to
fouling (Wahl, 1989). Although fouling organisms can be
beneficial to their hosts, for example by offering camouflage
and by providing protection from predators by their second-
ary metabolites (Laudien and Wahl, 1999), the interaction is
largely considered harmful. Among the negative effects are
increased hydrodynamic drag on the host, which can lead to
dislodgment of sessile hosts; and disruption of the host’s
feeding, either by direct competition for food particles or by
changing the water flow to the host, which is especially
important for filter-feeding organisms (Stoecker, 1978;
Wahl, 1989; Krug, 2006).
Ascidians (phylum: Chordata, subphylum: Tunicata) are
soft-bodied, sessile, filter-feeding organisms. They occur in
all oceans in colonial and solitary forms. Fouling on ascid-
ians can lead to the obstruction of the inhalant and exhalant
siphons as well as to the clogging of the branchial basket,
important to both respiration and feeding (Lambert, 1968;
Koplovitz et al., 2011). Both naturally fouled and non-
fouled ascidian species have been reported from various
geographical regions (e.g., Stoecker, 1980; Uriz et al., 1991;
Davis and White, 1994). Fouled ascidian species might use
behavioral responses (e.g., actively closing the siphons or
squirting water and particles from the branchial basket
through apertures [Hoyle, 1953]) and physical responses
(e.g., regular tissue sloughing [Goodbody, 1962] and mucus
secretion [Wahl et al., 1998]) to overcome fouling. Short-
lived ascidians might be able to grow and reproduce before
becoming fouled (Stoecker, 1980). Among the taxa reported
as epibionts on ascidians are bacteria, algae, bryozoans,
Received 25 September 2013; accepted 5 September 2014.
* To whom correspondence should be addressed. E-mail: bmayzel@
gmail.com
Reference: Biol. Bull. 227: 232–241. (December 2014)
© 2014 Marine Biological Laboratory
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