Marine Biology (2018) 165:107
Fluctuations in the strength of chemical antifouling defenses in a red
macroalga in response to variations in epibiont colonization pressure
· Florian Weinberger
· Mark Lenz
Received: 26 February 2018 / Accepted: 22 May 2018 / Published online: 4 June 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Marine macroalgae in temperate regions are constantly exposed to colonization by fouling organisms, but the intensity
of fouling ﬂuctuates in time. We, therefore, hypothesized that a macroalgal species from these latitudes should be able to
adjust its antifouling defense to the prevailing colonization pressure. To test this assumption, fouling pressure in the West-
ern Baltic Sea as well as the activity of surface extracts gained from the non-native Gracilaria vermiculophylla against the
diatom Stauroneis constricta and the ﬁlamentous alga Ceramium tenuicorne were assessed over one vegetation period on a
monthly basis. We used two solvents with diﬀerent polarities to extract chemical compounds from the alga. Both, hexane and
dichloromethane (DCM) surface extracts, inhibited settlement of C. tenuicorne, while only hexane surface extracts deterred
S. constricta. Furthermore, the activities of both extracts ﬂuctuated on the scale of months and the ﬂuctuations in the activ-
ity against C. tenuicorne, which were observed in DCM extracts, correlated with the intensity of fouling pressure that C.
tenuicorne inﬂicted on G. vermiculophylla in the ﬁeld. Thus, G. vermiculophylla appears to be able to adjust its antifouling
defenses—at least partly—to fouling pressure.
Epibiosis is the spatial association between an ‘epibiont’
(the fouling organism) and a ‘basibiont’ (the fouled host
organism), which is typical and ubiquitous in marine envi-
ronments (Taylor and Wilson 2003; Wahl 1989). Seaweeds
are photosynthetic organisms and particularly prone to colo-
nization by epibionts, which comprise many diﬀerent taxa
from all kingdoms, as they are sessile and restricted to the
shallow, euphotic zone where the abundance and diversity
of fouling organisms are known to be high (da Gama et al.
2008; de Nys et al. 1995).
Although epibionts have not only detrimental, but also
neutral or even beneﬁcial eﬀects on the basibiont seaweeds
(Costerton et al. 1987; Thevanathan 2000), they are gen-
erally considered harmful for the performance of the host
(Duﬀy and Hay 2000; Wahl 2008). These eﬀects can be
direct or indirect. A direct inﬂuence is given when epi-
bionts reduce growth and photosynthesis of the host alga
by competing with it for light and nutrients (Cebrian et al.
1999; Honkanen and Jormalainen 2005), when they impair
the host by mechanically penetrating into the tissues (Leon-
ardi et al. 2006), or when they cause mortality by increasing
drag and weight (Hemmi et al. 2005). Indirect eﬀects emerge
when palatable epibionts increase the attractiveness of the
host alga for consumers (Wahl et al. 1997). Such negative
eﬀects on macroalgal ﬁtness should lead to the selection of
genotypes that possess an eﬃcient antifouling defense that
minimizes surface colonization (Clare 1996; da Gama et al.
2014; Nylund et al. 2008; Paul and Ritson-Williams 2008).
This concept was recently and for the ﬁrst time conﬁrmed in
a study on the perennial red alga Gracilaria vermiculophylla
(Ohmi) Papenfuss (Wang et al. 2017a, b). Within this spe-
cies, individuals from non-native populations, which had
successfully established in European coastal waters, exhib-
ited a stronger capacity to inhibit settlement of diatoms and
Responsible Editor: M.Y. Roleda.
Reviewed by B. A. Perez Da Gama and G. Culioli
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s0022 7-018-3365-4) contains
supplementary material, which is available to authorized users.
* Shasha Wang
Department of Benthic Ecology, GEOMAR Helmholtz-
Zentrum für Ozeanforschung Kiel, 24105 Kiel, Germany