Marine Biology (2006) 148: 11931199

DOI 10.1007/s00227-005-0167-2

R ES E AR C H A RT I C L E

Gunilla B. Toth Henrik Pavia

Artificial wounding decreases plant biomass and shoot strength

of the brown seaweed Ascophyllum nodosum (Fucales, Phaeophyceae)

Received: 26 May 2005 / Accepted: 5 October 2005 / Published online: 26 November 2005

Springer-Verlag 2005

Abstract Brown seaweeds can serve as habitat and food

for a number of mesoherbivore species, but the eect of
mesoherbivore grazing on the tness of individual seaweed plants is not well documented. Here we investigate
how mechanical wounding, which mimics the grazing
damage made by the herbivorous gastropod Littorina
obtusata, aects the biomass change, apical growth, and
individual shoot strength of the fucoid seaweed species
Ascophyllum nodosum both in natural eld populations
and in the laboratory. We did not detect a signicant
eect of wounding on apical shoot growth in the laboratory, but wounding decreased the plant biomass in
half of the studied A. nodosum populations in the eld.
Furthermore, we found that the strength of individual
A. nodosum shoots was signicantly lower when compared with unwounded control shoots initially after
wounding. However, after 11 days incubation in the
laboratory, the strength of the wounded shoots had increased almost to the level of the control shoots, although there was still a signicant dierence in the force
required to break the shoots. These results indicate that
wounding can increase the tissue loss (and thereby decrease the tness) of A. nodosum plants in natural populations, probably through weakening of individual
shoots. However, A. nodosum appears to have a mechanism to strengthen the shoots after mechanical
wounding, and therefore, the timing of damage (e.g.
prior to a storm) probably determines the amount of
plant tissue lost through wave-induced forces.

Communicated by M. Kuhl, Helsingr

G. B. Toth (&) H. Pavia
Department of Marine Ecology,
Tjarno Marine Biological Laboratory, Goteborg University,
SE 452 96 Stromstad, Sweden
E-mail: gunilla.toth@tmbl.gu.se
Tel.: +46-526-68614
Fax: +46-526-68607

Introduction
Fucoids (Fucales) and kelps (Laminariales) are the most
conspicuous and abundant marine plants in temperate
areas around the world, where they can form extensive
underwater forests. The plants often serve both as habitat and food for a large diversity of small (<2.5 cm)
herbivorous gastropods and crustaceans, which are
called mesoherbivores (Brawley and Fei 1987). It has
been argued that mesoherbivores are not important
selective agents for seaweeds due to the fact that they
usually only remove a minor part of the plant biomass
through grazing (Hay and Steinberg 1992). However,
this reasoning is probably not valid because even if only
a minor part of the plant biomass is removed, grazing
can probably result in large negative tness consequences for the seaweeds depending on the feeding
behaviour of the herbivore species (Duy and Hay 2000;
Pavia and Toth 2000). For example, deep grazing
damage on the basal parts of the seaweeds may cause
increased risks of dramatic tissue losses due to breakage
of whole primary shoots (Padilla 1993). There is presently very little information available about the eects of
mesoherbivore grazing on the tness of seaweed individuals (Arrontes 1999). In particular, there are few
manipulative experimental studies on how tissue
wounding aects seaweed survival in natural populations (but see DeWreede et al. 1992; Markel and
DeWreede 1998; Duggins et al. 2001).
Seaweeds have evolved a wide range of strategies to
avoid the negative eects of herbivory, for example,
escape in time or space, tolerance by increased growth
or reproduction, and resistance through morphological
and chemical defences (Duy and Hay 1990). Defences
can be expressed constitutively, or may be induced in
response to herbivore-specic cues (Amsler 2001). For
example, the brown seaweed Ascophyllum nodosum (L.)
Le Jol. induces a chemically based herbivore resistance
in response to both direct grazing by the herbivorous
snail Littorina obtusata (L.) and to water-borne signals

1194

from gastropods feeding on conspecic seaweeds

(Pavia and Brock 2000; Pavia and Toth 2000; Toth
and Pavia 2000; Borell et al. 2004). However, direct
grazing by the crustacean Idotea granulosa Rathke and
articial wounding does not induce this response
(Pavia and Toth 2000). On the other hand, A. nodosum
fronds have previously been shown to induce increased
strength and toughness in response to articial damage
(Lowell et al. 1991), indicating that the seaweed has a
mechanism to minimize tissue loss after wounding.
In the present study, we investigated how the biomass
change, apical growth, and shoot strength of A. nodosum
are aected by articial wounding that structurally
mimics the grazing damage made by L. obtusata.
Reduction in individual size through losses of whole
primary shoots has large negative tness consequences
for A. nodosum (Pavia et al. 2002), and therefore tness
was correlated both to biomass changes of A. nodosum
plants in natural eld populations and to shoot growth
in the laboratory. We specically hypothesized (1) that
plants that were articially wounded would lose more
biomass compared with the unwounded control plants
in the eld, (2) that wounded plants would grow less
compared with the unwounded plants in the laboratory,
(3) that the strength of wounded A. nodosum shoots
would be less compared with the unwounded shoots
initially after wounding, and (4) that the wounded
shoots would increase in strength after a period of time.

Materials and methods

Study organism
A. nodosum is a common fucoid seaweed species that
can form large monospecic stands in the intertidal
zone of sheltered North Atlantic rocky shores. An
individual consists of several genetically identical primary shoots that arise from a common holdfast and
that branch into secondary shoots as the individual
grows (Fig. 1a). It shows apical growth with dichotomous lateral branching and new air bladders are
formed at the tip of the shoots every spring, which
allows for separation of the primary shoots into age
classes. The shoots can be upto 2 m long and
>20 years old, but are often broken especially at the
point of herbivore damage (Viejo and Aberg 2001).
The reproductive structures (receptacles), which grow
from pits along the sides of the primary shoots, rst
appear in June, develop during the year, and are shed
shortly after the release of gametes in May the following year.
A. nodosum is commonly inhabited by a community
of mesoherbivores consisting mainly of gastropods,
isopods, and amphipods (Pavia et al. 1999). One of the
most abundant herbivores is the gastropod L. obtusata,
which is specialized to live and feed on A. nodosum
and a few other fucoid seaweed species (Vermeij 1992;
Watson and Norton 1987). The radula teeth of

L. obtusata have shovel-like cusps (Steneck and Watling 1982; Watson and Norton 1987), which causes
concentrated and deep damage that often results in
round holes right through the seaweed thallus
(Fig. 1b). Furthermore, L. obtusata is most abundant
on the lower parts of the A. nodosum thallus, probably
because there is less chance of detachment compared
with the narrower apical shoots (Watson and Norton
1987). This means that wounding caused by L. obtusata attacks may result in losses of whole primary
shoots, especially during periods of wave-induced drag.
Field experiment
The biomass change of articially wounded A. nodosum
plants in natural eld populations was investigated
outside the Tjarno Marine Biological Laboratory
(TMBL, 5854N, 1107E) on the Swedish west coast in
May 2001. Twenty A. nodosum individuals were collected haphazardly from each of the four dierent sites
outside TMBL by carefully removing the holdfasts
from the substratum, and were brought back to the
laboratory. Half of the plants from each site (i.e. a
total of 40 plants) were subjected to wounding with a
hole-punch in order to mimic L. obtusata grazing
damage (Fig. 1b). Natural densities of L. obtusata may
remove upto 15% of the initial plant wet weight during
a period of 4 weeks in the laboratory (Pavia and Toth
2000) and can also decrease the individual net plant
growth during the main period of growth with a signicant 50% in natural seaweed populations (Toth GB,
Karlsson M, Pavia H, unpublished). Wounding was
performed by punching holes with a diameter of
35 mm dispersed over the seaweed thallus until 7% of
the initial plant wet weight had been removed. The
amount of biomass removed was chosen to correspond
to about 2 weeks grazing by L. obtusata (Pavia and
Toth 2000). The remaining plants were kept as controls
and were, besides the actual wounding treatment,
treated the same way as the wounded plants. Because it
was anticipated that the seaweeds would release their
gametes and shed the receptacles during the course of
the experiment, all receptacles were removed from each
individual and the wet weight of the plants was determined. This procedure ensured that a correct estimate
of the thallus wet weight was obtained at the start of
the experiment. The plants were transplanted back to
their original growing site, and were anchored with
plastic cable ties to the primary shoots of an already
attached plant with all its secondary shoots removed
10 cm above the hold-fast. After 12 days, all plants
were collected and their wet weights were determined.
Seaweed wet weight changes during the course of the
experiment were calculated as percentage of the initial
wet weight. Data were statistically analysed using a
two-way analysis of variance (ANOVA) with wounding
as a xed two-level factor, and site as a random fourlevel factor.

1195
Fig. 1 a A. nodosum
morphology. The plants are
attached to the substratum with
a holdfast from which one to
several primary shoots arise.
The primary shoots, which
branch into secondary shoots as
the individual grows, show
apical growth with
dichotomous lateral branching
and new air bladders are
formed at the tip of the shoots
every spring, allowing for
separation of the shoots into
age classes. The reproductive
structures (receptacles) grow
from pits along the sides of the
shoots; b L. obtusata, grazing
damage, and articial wounds.
The radula teeth of L. obtusata
have shovel-like cusps, which
make deep and concentrated
damage that results in round
holes through the A. nodosum
thallus. Articial wounding,
which structurally mimics the
L. obtusata grazing damage,
was made with a hole-punch

Twenty A. nodosum shoots were collected from haphazardly chosen sites outside TMBL in May 2001. The
shoots were cut between the air bladders that were
formed during the years 1998 and 1999, that is, all
shoots were the same age (3-years-old) and were
approximately 1520 cm long. In half of the shoots
(n=10), ten holes with a diameter of 3 mm were punched below the oldest air bladder, and one hole was
punched in the air bladder that was formed during the
year 2000. The rest of the shoots were kept as controls
and were not wounded. The shoots were placed individually in aquaria supplied with running seawater
outside the laboratory. The length of the apical part of
the shoots (i.e. above the last air bladder) was measured
at the start and at the end of the 18-day experiment. The
growth of the apical shoots was calculated as per cent
increase of the initial length. Data were statistically
analysed using a one-way ANOVA with wounding as a
two-level factor.

(n=20) was measured at the beginning of the experiment

with a spring scale. The shoots were tied to the scale,
slowly pulled towards the experimenter until they were
torn, and the maximum weight registered on the spring
scale was noted. The rest of the shoots were placed in
aquaria in the laboratory for 11 days, after which the
strength was measured using the same procedure as for
the initial measurements. The weight deviations noted
from the spring scale were then converted to force (F)
using the formula F=mg, where m is the weight registered on the spring scale, and g is the acceleration due to
gravity (9.82 ms 2). The strength of the shoots was related to the force required to break the shoots. Data were
statistically analysed in a two-way ANOVA with
wounding and time as xed two-level factors.
Before all statistical analyses, the homogeneity of
variances was tested with Cochrans test (Underwood
1997). The variances in all experiments were homogenous and data were not transformed. Means were
compared using the Student-Newman-Keuls (SNK)
multiple comparisons test (Underwood 1997).

Thallus strength

Results

Eighty 3-year-old A. nodosum shoots (1520 cm) were

collected from haphazardly chosen sites in the Tjarno
archipelago in May 2001. Half of the shoots were
exposed to wounding by punching three holes with
a diameter of 3 mm in the base of the shoots in a
standardized way to mimic L. obtusata grazing damage.
The rest of the shoots were kept as controls. The strength
of half of the wounded and half of the control shoots

Field experiment

Growth of apical shoots

There was a signicant loss of biomass from wounded

A. nodosum plants in two of the four experimental sites, as
shown by the statistically signicant interaction between
the factors wounding and site (Table 1). The control
plants all had a net increase in biomass on an average of
about 10% of the initial wet weight during the 12-day

1196
Table 1 Field experiment. Analysis of variance of the wet weight change (of initial wet weight) of unwounded and articially wounded A.
nodosum plants 12 days after transplantation to four dierent eld sites. Data on mean values and SE can be found in Fig. 2
Source of variance

df

MS

F versus

Wounding
Site
Wounding Site
Residual

1
3
3
68

6043.03
1571.89
1906.01
457.20

3.17
3.44
4.17

0.173
0.021
0.009

Wounding Site
Residual
Residual

experiment, while the biomass of the wounded plants at

sites 1 and 2 (Langholmen and Salto Lygnholmen) decreased with a signicant 14 and 27%, respectively (SNKtest, P<0.05, Fig. 2). The wet weight change for the
wounded plants at sites 3 and 4 (Lilla Flatskar and Yttre
Burholmen) was not signicantly dierent from the
control plants (SNK-test, P>0.05, Fig. 2).

signicantly (SNK-test, P<0.05) during the course of

the experiment (Fig. 4). However, although the wounded shoots increased, and the control shoots decreased,
in strength during the experiment, the control shoots
were still signicantly stronger compared with the
wounded shoots when the experiment was terminated,
but the relative dierence in strength had decreased from
170 to 20%.

Growth of apical shoots

There was no statistically signicant dierence in growth
between A. nodosum shoots that had been wounded and
unwounded control shoots (ANOVA, F1,18=0.14,
P=0.71). The mean length of the apical shoots increased
by 9.5% during the 18-day experiment (Fig. 3).

Discussion and conclusions

Induction of chemically mediated herbivore resistance in
seaweeds has only been found in response to grazing by

Thallus strength
There was a statistically signicant interaction between
the factors wounding and time (Table 2) when the
strength of the wounded and control A. nodosum shoots
was studied. The wounding initially decreased the mean
strength of the A. nodosum shoots by a statistically
signicant (SNK-test, P<0.05) 62% (Fig. 4). However,
after 11 days the mean strength of the damaged shoots
had increased by 150% compared with their initial
strength after wounding (Fig. 4). The strength of the
control shoots, on the other hand, decreased slightly but
Fig. 3 Growth of apical shoots. Growth (per cent of initial shoot
length) of unwounded (control) and articially wounded (wounding) 3-year-old A. nodosum shoots after 18 days incubation in
outdoor aquaria supplied with running seawater. A total of 11
holes (3 mm) were made in the base and air bladder of the shoots
with a hole-punch in order to mimic grazing by L. obtusata. Error
bars represent SE (n=10)

mesoherbivores (e.g. Cronin and Hay 1996; Pavia and

Fig. 2 Field experiment. Wet weight change (per cent of initial wet
weight) of unwounded (control) and articially wounded (wounding) A. nodosum plants 12 days after transplantation to four
dierent eld sites. The articially damaged plants had 7% of the
wet weight removed by making 35-mm holes distributed evenly
over the entire seaweed thallus prior to transplantation. Letters
above bars indicate statistically signicant dierences between
mean values based on the SNKs multiple comparisons test
(P<0.05). Error bars represent SE (n=20)

Table 2 Thallus strength. Analysis of variance of the force (N)

required for breaking unwounded and articially wounded 3-yearold A. nodosum shoots at two sampling times (0 and 11 days) after
incubation in running seawater in the laboratory. Data on mean
values and SE can be found in Fig. 4
Source of variance

df

MS

Wounding
Time
Wounding Time
Residual

1
1
1
76

1.79
0.33
0.73
0.08

20.14
3.74
8.25

<0.001
0.057
0.005

1197

Fig. 4 Thallus strength. Force (N) required for breaking unwounded (control) and articially wounded (wounding) 3-yearold A. nodosum shoots initially after damage (0 days) and after
11 days incubation in running seawater in the laboratory. Three
holes (diameter=3 mm) were made in the base of the shoots with a
hole-punch to mimic grazing by L. obtusata. Letters above bars
indicate statistically signicant dierences between mean values
based on the SNKs multiple comparisons test (P<0.05). Error
bars represent SE (n=20)

Toth 2000; Toth and Pavia 2000; Sotka et al. 2002;

Taylor et al. 2002; Borell et al. 2004; Rhode et al. 2004;
Weidner et al. 2004), indicating that mesoherbivores may
exert a signicant selection pressure on the seaweeds. The
results show that articial wounding with a hole-punch,
which structurally mimics the grazing damage from L.
obtusata, had no statistically signicant eect on the
apical growth of A. nodosum shoots. On the other hand,
articial wounding corresponding to the amount of tissue removed by natural densities of the herbivorous
gastropod L. obtusata, signicantly increased the loss of
plant biomass in natural populations. However, this only
applied to two of the four study sites, while at the other
two sites, no eect on biomass was detected. The dierence between sites is probably due to interactions between the tissue damage and other factors, for example,
desiccation (e.g. Haring et al. 2002), or wave-induced
tearing (e.g. Lowell et al. 1991). In contrast to A. nodosum that only grows on sheltered shores, most previous
studies on the interactive eects of tissue damage and
ow has been performed on kelp species that grow in
high-ow environments. The eect of ow on dierent
kelp species can be highly inuenced by herbivore damage made by sea urchins (e.g. Tegner et al. 1995), and
gastropods (e.g. Markel and DeWreede 1998; Duggins
et al. 2001). The area where the present study was conducted is atidal (tidal range <30 cm) and changes in
water levels are mainly driven by wind and/or air pressure. The study area consists of a number of small islands
situated outside the mainland, and there is a complex
pattern of currents and wave regimes in the narrow
sounds between the islands, which make predictions of
water movements dicult. There was no apparent difference in exposure between the experimental sites used
in the present study, that is, they all faced away from the
predominant wave direction and are thus considered as
sheltered shores. However, exposure was not quantied

and dierences in wave- or current-induced forces may

have been responsible for the dierent eects of tissue
wounding on plant tness at dierent sites found in the
present study.
The results show that articial damage initially decreased the strength of the A. nodosum shoots. However,
after incubation in indoor aquaria, the strength of the
wounded shoots increased while the strength of the
control shoots decreased. The shoots were kept with
continuous supply of fresh seawater and appeared healthy throughout the experiment. However, the decease in
control shoot strength over time may be a result of the
articial physical environment (e.g. lower light intensity)
in the aquaria. Therefore, the signicant increase in
strength of the wounded shoots strongly implies that A.
nodosum has an active mechanism to strengthen the
shoots after mechanical damage. The results are in
accordance with an earlier study where the strength and
toughness of A. nodosum fronds decreased initially after
articial damage, but increased signicantly after
4 weeks in the eld, indicating that the seaweeds induced
a morphological defence in response to articial damage
(Lowell et al. 1991). In contrast, the strength of three kelp
species was not increased 6 months after articial damage made with a razor blade, although the authors observed tissue re-growth in all species (DeWreede et al.
1992). These results indicate that kelps and fucoids may
have dierent strategies when dealing with tissue damage
made by herbivores, but more studies are needed before
taxonomic patterns of induced morphological defences
in seaweeds can be revealed.
Attempt was not made to section through the
wounded A. nodosum plants to investigate possible tissue
re-growth or other structural changes at the cell level at
the site of wounding. However, Luder and Clayton
(2004) performed a microscopic study of the woundhealing process of the kelp Ecklonia radiata after articial damage with a cork borer and found three dierent
stages; (1) new medullar cells were formed to close the
medulla, (2) physodes containing phlorotaninns (polyphenols) started to accumulate at the wound site, and
(3) a new epidermis was formed by dierentiation of the
medullar cells. Similar wound-healing processes were
also observed in the fucoid seaweeds Sargassum (Fagerberg and Dawes 1976, 1977) and Fucus (Fulcher and
McCully 1969, 1971). The strength of the wounded
seaweed tissues were not tested in the microscopic
studies (Fulcher and McCully 1969, 1971; Fagerberg
and Dawes 1976, 1977; Luder and Clayton 2004), but it
is likely that formation of new tissue and cross-linking of
phlorotannins in the cell walls (Luder and Clayton 2004)
is contributing to the increased strength of wounded A.
nodosum shoots found in this study and in the previous
study by Lowell et al. (1991).
L. obtusata is a relatively sedentary herbivore that
must feed for a relatively long period of time (2 weeks,
Pavia and Toth 2000) in order to consume about the
same amount of biomass that was experimentally removed with the hole-punch before transplanting the

1198

plants back to their original growing sites in the eld

experiment. The fact that A. nodosum is able to induce a
morphological defence by strengthening the shoots at
the site of wounding within 11 days strongly suggest that
the biomass loss found in two of the four sites could
have been unnaturally high because all plant damage in
the eld experiment was made within a very short period
of time. On the other hand, it is probably enough with
one or a few tissue wounds from a snail to tear a shoot,
and shoots in the eld are usually torn at the site of
grazing damage (Viejo and Aberg 2001). L. obtusata is
able to graze through the thallus of A. nodosum within a
day in outdoor aquaria supplied with ow-through
seawater (Toth G, personal observation), indicating that
grazing damage could contribute signicantly to the loss
of seaweed shoots, especially during periods of strong
wave-action. In a eld experiment, plants growing at
sites where littorinid snails were experimentally removed
had twice as large long-term net growth as plants
growing in sites with natural snail densities (Toth GB,
Karlsson M, Pavia H, unpublished) indicating that
herbivorous gastropods can have a signicant negative
eect on plant tness in the eld.
In conclusion, it was found that articial wounding,
which structurally mimics the grazing damage made by
L. obtusata, can result in a signicant biomass loss of
individual A. nodosum plants in natural populations.
Because the tness of A. nodosum is tightly coupled to
plant size (Pavia et al. 2002), this type of damage can
probably have signicant negative eects on the individual tness of this seaweed species. The tissue loss is
probably due to a combination of weakening of the
shoots due to damage and wave-induced forces on the
shoots. Although A. nodosum appears to have a mechanism to increase the shoot strength in response to
articial damage, the strength of wounded shoots was
still lower compared with the control shoots after
11 days. The negative eect of grazing damage on A.
nodosum plants in the area where this study was conducted is probably highly dependent on stochastic
events, such as storms.
Acknowledgements We are grateful to C. Appelqvist, M. Hemmingsson, H. Johansson, O. Langhamer, and J. Lycken for practical assistance and fruitful discussions. The experiments performed
in the present study comply with current Swedish laws. This study
was supported by the European Union through The European
Regional Development Fund (ERDF) Objective 2 West Sweden
and through the Swedish Research Council through contract no.
621-2003-2883 to GT and 21.0/2003-1122 to HP.

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