Biol Invasions
DOI 10.1007/s10530-010-9913-6
ORIGINAL PAPER
Effects of invasive seaweeds on feeding preference
and performance of a keystone Mediterranean herbivore
Fiona Tomas • Antonio Box • Jorge Terrados
Received: 12 July 2010 / Accepted: 16 November 2010
Ó Springer Science+Business Media B.V. 2010
Abstract The consequences of invasive species on
ecosystem processes and ecological interactions
remain poorly understood. Predator–prey interactions
are fundamental in shaping species evolution and
community structure and can be strongly modified by
species introductions. To fully understand the ecological effects of invasive species on trophic linkages it is
important to characterize novel interactions between
native predators and exotic prey and to identify the
impacts of invasive species on the performance of
native predators. Although seaweed invasions are a
growing global concern, our understanding of invasive
algae—herbivore interactions is still very limited. We
used a series of feeding experiments between a native
herbivore and four invasive algae in the Mediterranean
Sea to examine the potential of native sea urchins to
consume invasive seaweeds and the impacts of
invasive seaweed on herbivore performance. We
found that three of the four invasive species examined
are avoided by native herbivores, and that feeding
behaviour in sea urchins is not driven by plant
nutritional quality. On the other hand, Caulerpa
racemosa is readily consumed by sea urchins,
but may escape enemy control by reducing their
performance. Recognizing the negative impacts of
C. racemosa on herbivore performance has highlighted an enemy escape mechanism that contributes
to explaining how this widespread invasive alga,
which is preferred and consumed by herbivores, is not
eradicated by grazing in the field. Furthermore, given
the ecological and economic importance of sea
urchins, negative impacts of invasive seaweeds on
their performance could have dramatic effects on
ecosystem function and services, and should be
accounted for in sea urchin population management
strategies.
Keywords Plant—herbivore interactions Biotic
resistance Caulerpa racemosa Enemy release
hypothesis Seagrass Sea urchin
Introduction
F. Tomas (&) J. Terrados
Instituto Mediterráneo de Estudios Avanzados IMEDEA
(CSIC-UIB), C/Miquel Marques 21, 07190 Esporles,
Illes Balears, Spain
e-mail: [email protected]
A. Box
Laboratorio de Biologı́a Marina, Universidad Islas
Baleares—IMEDEA, Ctra. Valldemossa Km 7.5,
07122 Palma de Mallorca, Illes Balears, Spain
Invasive species are a major threat to the conservation of ecosystems and global biodiversity (Vitousek
et al. 1997; Mack et al. 2000). While their negative
effects on species diversity and abundance have been
widely documented, the effects of invasive species on
ecosystem processes are much less clear (Levine
et al. 2003, Rilov 2009). For instance, two conflicting
hypotheses predict opposite effects of invasive
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F. Tomas et al.
species on predator–prey interactions (Mitchell et al.
2006), which are known to structure ecological
communities (Power 1992; Borer et al. 2006) and
influence species evolution (Yoshida et al. 2003). On
the one hand, the enemy release hypothesis (ERH)
predicts that an introduced species will successfully
spread in a new environment lacking natural predators and is often proposed to explain invasive success
(Keane and Crawley 2002). Conversely, the biotic
resistance hypothesis (Elton 1958) suggests that
introduced plants are poorly adapted for deterring
native consumers, which limits their invasiveness. A
key step in understanding and predicting how introduced species may modify trophic linkages is to
characterize the novel interactions between native
predators and exotic prey. Furthermore, considering
that many introduced species become persistent
features of the new ecosystems they invade, it is
important to understand how they can potentially
modify ecological processes within these systems.
Invasive seaweeds are a major global concern,
since over 400 introduction events have been documented worldwide. They are known to deeply modify
marine ecosystems, and they can have strong detrimental ecological and economic impacts (Schaffelke
et al. 2006, Williams & Smith 2007, Thomsen et al.
2009). Surprisingly, our knowledge of invasive
algae—herbivore interactions is very limited and
mostly reduced to two species, namely Caulerpa
taxifolia and Codium fragile tomentosoides (e.g.,
Trowbridge 1995; Boudouresque et al. 1996; Thibaut
et al. 2001; Gollan and Wright 2006; Sumi and
Scheibling 2005; Scheibling et al. 2008).
Generalist herbivores can feed on numerous species, potentially incorporating exotic plants and
contributing to invasion control (Parker et al. 2006).
However, plants have evolved numerous strategies to
reduce herbivory such as decreasing attractiveness to
herbivores and diminishing herbivore performance.
Such defence mechanisms often function simultaneously and involve morphological, structural, and
chemical adaptations (Lubchenco and Gaines 1981;
Duffy and Hay 1990). For instance, higher quality
foods are generally preferred when available (e.g.,
Duffy and Paul 1992; Goecker et al. 2005), and tend
to enhance fitness (e.g., Cruz-Rivera and Hay 2000;
Berner et al. 2005), although consumers may increase
foraging to compensate for low quality food (i.e.,
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compensatory feeding; e.g., Simpson and Abisgold
1985; Valentine and Heck 2001; Berner et al. 2005).
In addition to assessing feeding behaviour of
native herbivores on invasive plants, it is also
important to identify the impacts of invasive species
on the performance (e.g., survival, growth, reproductive potential) of native fauna to fully understand the
ecological effects of invasive species (Wright and
Gribben 2008; Tallamy et al. 2010). This will be of
special concern to environmental managers when the
native fauna involved are strong interactors (sensu
Paine 1992), whose changes in abundance can have
dramatic impacts on community structure and function. For instance, sea urchins are one of the most
important generalist herbivores in tropical and temperate marine systems (Gaines and Lubchenco1982;
Lawrence 2001), and can play a fundamental role in
regulating marine invasions (e.g., Scheibling and
Gagnon 2006 and references therein). In addition,
many sea urchin species are of significant commercial interest in the fishing and aquaculture industries
worldwide (Lawrence 2001). Therefore, negative
impacts of invasive seaweeds on their performance
could have further detrimental consequences for
human services.
The Mediterranean Sea is the most invaded region
in the world in terms of exotic seaweeds (Williams
and Smith 2007), due to the construction of the Suez
Canal, intense marine traffic, and aquaculture (Galil
2008). In this study we investigated the influence of
four of the main exotic seaweeds (Caulerpa racemosa var. cylindracea, Lophocladia lallemandii, Acrothamnion preissii, and Womersleyella setacea)
invading Western Mediterranean subtidal ecosystems, particularly seagrass beds, on the feeding
behaviour and performance of the main keystone
native herbivore: the sea urchin Paracentrotus lividus
(Lamarck). We assessed whether marine generalist
herbivores such as sea urchins can consume invasive
seaweeds and potentially provide biotic resistance to
native communities. Specifically, we conducted a
series of feeding assays to obtain direct evidence of
the feeding preferences of native sea urchins for
different invasive seaweeds. In addition, we also
carried out a no-choice feeding experiment to assess
the impact of a readily eaten invasive species on
herbivore performance. Finally, we analyzed plant
traits to understand how nutritional quality drives the
Effects of invasive seaweeds on feeding preference and performance
feeding and performance patterns observed in sea
urchins.
Materials and methods
Study system and species
Four exotic algae have largely invaded the benthic
ecosystems of the Western Mediterranean (Boudouresque and Verlaque 2002; Occhipinti-Ambrogi et al.
2010): the green alga Caulerpa racemosa var.
cylindracea (hereafter C. racemosa), and the Rhodophytes Lophocladia lallemandii, Acrothamnion preissii, and Womersleyella setacea. These exotic algae
have high rates of spread (Piazzi et al. 2005; Cebrian
and Ballesteros 2010) and strong deleterious effects
on native seagrass and algal communities (e.g., Piazzi
and Cinelli 2001; Ballesteros 2006; Ballesteros et al.
2007; Piazzi and Balata 2008; Deudero et al. 2010).
The endemic seagrass Posidonia oceanica is a
widespread foundation species in the Mediterranean,
creating extensive meadows from 0 to ca. 45 m depth
(Procaccini et al. 2003). P. oceanica beds exhibit
high primary productivity, provide habitat, refuge,
and trophic resources for numerous species, as well
as having a key role in coastal protection and carbon
fixation (Pergent et al. 1994; Romero 2004). As a
result of their ecological importance, P. oceanica
beds are protected habitats within the European
Habitats Directive (92/43/CEE). Like other seagrass
ecosystems, P. oceanica beds are suffering severe
decline due to human activities and are also
threatened by increasing numbers of invasive species
(Boudoresque et al. 2009).
The edible sea urchin Paracentrotus lividus is the
main generalist herbivore in the Western Mediterranean having a paramount role in controlling the
structure of subtidal benthic communities, and it is
generally found at densities between 0 and 6 ind. m-2
in seagrass beds and around 10–30 ind. m-2 in rocky
substrates (Boudouresque and Verlaque 2001). When
inhabiting P. oceanica beds, sea urchins mainly
consume seagrass blades (Tomas et al. 2005a; 2006)
and, at high densities (e.g., 12–25 ind. m-2), they can
transform dense meadows into barrens (e.g., Ruiz et al.
2009). In addition, this species is fished extensively in
many parts of Europe, where the high demand for
human consumption has triggered the development of
an important aquaculture market in France, Ireland and
Spain (Boudouresque and Verlaque 2001). Under
stressful conditions (limiting food, competition, etc.),
sea urchins commonly exhibit changes in their performance through the modification of certain biological
parameters. Both somatic (e.g., changes in body size or
in the size of the feeding apparatus) and reproductive
(quantity and quality of gonads) changes are commonly detected (e.g., Ebert 1968, 1980; Levitan 1991;
Fernandez and Boudouresque 1997; Tomas et al.
2005b).
Other than C. taxifolia, susceptibility of invasive
algae to Mediterranean herbivores has received little
attention. Although sea urchins can ingest C. racemosa (Ruitton et al. 2006; Žuljević et al. 2008), they
are only capable of partially limiting its growth and
cover, or can even favour its spread (Bulleri et al.
2009; Cebrian et al. in press). The absence of other
invasive algae from sea urchin and other herbivore’s
gut contents (Ruitton et al. 2006; Box et al. 2009;
Cebrian et al. in press) would suggest that these
species may be avoided by herbivores, although no
direct evidence is available.
Herbivore feeding behaviour and performance
Feeding preference
To assess the capacity of native herbivores to
consume and potentially regulate invasive seaweeds,
we performed feeding preference assays in which sea
urchins were offered a choice between the native
species P. oceanica and one of the invasive algae
(C. racemosa, L. lallemandii, W. setacea or A. preissii).
Feeding assays were conducted under controlled
aquaria conditions in a constant-temperature room
kept at 19°C. Sea urchins were acclimatized to
laboratory conditions for 48 h before starting each
assay, during which they were fed freshly collected
Ulva sp. Each sea urchin was placed in an individual
aerated tank, which was divided into 2 compartments
by a fine mesh (250 lm), one of which contained the
pertinent no-herbivore control (i.e., macrophytes
without sea urchin) to account for autogenic changes
in seagrass and algal material. Urchins were offered
similar amounts of freshly collected alga and seagrass
biomass (collected the morning of the experiment),
which were blotted dry of excess water before
measuring initial and final wet weight. Assays were
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F. Tomas et al.
terminated when ca. half of one treatment had been
consumed. Biomass consumption was estimated as
[(Hi 9 Cf/Ci) - Hf], where Hi and Hf were initial and
final wet masses of tissue exposed to herbivores, and
Ci and Cf were initial and final masses in paired
controls (Parker and Hay 2005). Between fifteen and
twenty replicates were conducted per assay, and
replicates in which all food was consumed or where
urchins failed to feed were discarded in statistical
analyses since they do not provide information on
feeding preference.
No-choice feeding experiment
We detected a strong feeding preference towards the
invasive alga C. racemosa in our assays (see
‘‘Results’’). Studies indicate that sea urchins can
ingest substantial amounts of this species, but they
cannot limit its spread (Bulleri et al. 2009; Cebrian
et al. in press). We therefore hypothesized that
C. racemosa may be escaping herbivores not by
reducing their preference, but, perhaps, by reducing
their performance. Thus, we experimentally determined the effects of feeding on the invasive species
C. racemosa vs. the native seagrass P. oceanica on
key performance traits of sea urchins (Levitan 1988,
1991; Tomas et al. 2005b) by conducting a no-choice
experiment. Sea urchins were fed either native or
invasive plant material over a 3-month period, which
was deemed sufficient to capture diet-related changes
in biological parameters for P. lividus (e.g., Boudouresque et al. 1996; Cook and Kelly 2007). During
this experiment we also measured consumption rates
to elucidate whether compensatory feeding might be
taking place (e.g., Cruz-Rivera and Hay 2001).
The experiment was conducted in the facilities of
Palma Aquàrium, Palma de Mallorca, using a
constant-temperature (21°C) seawater flow-through
system. Three large tanks (300 L) were divided using
Plexiglas, to obtain a crossed design (diet 9 tank).
Sea urchins were collected in July 2008 and randomly
distributed among tank compartments. Furthermore,
15 additional individuals from the initial population
were kept and frozen to obtain a reference of sea
urchins’ biological conditions at the beginning of the
experiment.
Each compartment corresponded to a replicate of
one experimental treatment containing eight sea
urchins, which were fed fresh material twice a week
123
(ca. 50 g wet weight). To correct for biomass losses
due to autogenic changes in plant material, controls
without sea urchins were set within each compartment. Biomass consumed was measured following
Parker and Hay (2005, see above) during 13 sampling
events throughout the experiment.
At the completion of the experiment (October
2008), sea urchins from all compartments were
collected and frozen. We examined survivorship,
growth, fecundity and size of the feeding apparatus as
measures of sea urchin performance. In the laboratory, experimental sea urchins, as well as those
collected at the beginning of the experiment, were
measured using callipers and dissected into the
following components: gonads, Aristotle’s lantern
(feeding apparatus), and test. Each was dry-weighed
(60°C until constant weight), and used to calculate
the relation between body parts. The indices calculated (Tomas et al. 2005b) were:
Gonadal Index (GI) GI ¼ ðDW of 5 gonads/
DW of bodyÞ 100
(b) Aristotle’s lantern Index (LI) LI ¼ ðDW of
lantern/DW of bodyÞ 100
(a)
GI is considered to reflect reproductive performance (Vadas 1977), while LI is considered to reflect
investment in feeding (Ebert 1980, Levitan 1991).
Analysis of plant traits
To determine whether variation in plant traits related
to herbivore feeding preference and performance we
quantified nutritional traits of three of the species
offered on the feeding preference assays: the native
species (P. oceanica), a preferred invasive alga
(C. racemosa), and an avoided invasive species
(L, lallemandii).
To encompass potential temporal variations in
plant traits, plant material was collected three times
throughout the experimental period (July, August and
end of September). Once in the laboratory, seagrass
and algae were frozen, dried at 60°C until constant
weight (ca. 48 h) and ground into a fine powder. Each
sampling event was used as a sample, and consisted
of ca. 5 g wet weight of pooled material (i.e., several
seagrass shoots or algal thalli). Carbon and nitrogen
content (%DW) were measured using a CarloErba autoanalyzer. We also measured organic matter
Effects of invasive seaweeds on feeding preference and performance
content as the weight loss (%) after burning ca.
40 mg of the pooled dried sample for 6 h at 450°C.
All macrophytes and urchins used in this study
(i.e., for feeding choice and performance experiments, and for analyses of plant traits) were collected
around St Elm, Mallorca, Spain (39°340 4400 N,
2°200 5700 E) and were transported to the laboratory
in aerated seawater tanks.
Statistical analysis
For the feeding preference assays we analyzed the
percentage biomass consumed by means of Wilcoxon
signed-ranks paired test (due to lack of normality and
homoscedasticity of data). To assess the effects of the
different diet (native or invasive species) on sea
urchin consumption rates (% of biomass eaten) on the
no-choice feeding experiment, we used the Repeated
Measures ANOVA univariate method. The different
diet type (C. racemosa, P. oceanica) was the
between-subject factor and time (i.e., sampling
events) was the repeated measures (within-subjects)
factor. We used corrected significance levels from
Greenhouse-Geisser adjustment as recommended by
Quinn and Keough (2002).
To analyze the impacts of the different diets
(C. racemosa vs. P. oceanica) on sea urchin performance, we first conducted separate Two-Way ANOVAs for each biological parameter measured (Test
Diameter, GI, and LI) with a fixed factor (diet) and a
random factor (aquaria) (replicates were sea urchins).
There was no significant aquaria effect, nor significant aquaria x diet interaction (a [ 0.25, results not
shown), which allowed us to consider a model with
one factor (i.e., Diet) (using recommendations in
Quinn and Keough 2002 and references therein).
Thus, we performed separate One-Way ANOVAs
(factor diet) for each response variable (replicates
were urchins).
To compare nutritional quality of different macrophytes, we performed separate One-Way ANOVAs
with a fixed factor (species) for each variable (%C,
%N, C/N, and % organic matter). We also estimated
mean ingestion rates of C, N, and organic matter for
urchins fed different diets by multiplying the biomass
consumed during each experimental period by the
percentage of carbon, nitrogen and organic matter in
the food source. Ingestion data were analyzed as in
the case of the no-choice experiment, by means of
Repeated Measures ANOVA.
When overall significant differences were
detected, a posteriori pairwise comparisons of means
were performed using the Student–Newman–Keuls
[SNK] test. Prior to statistical analyses, normality and
homogeneity of variance were checked for all data
(Kolmogorov–Smirnov Test and Cochran’s test,
respectively). All differences were considered significant at P \ 0.05. Analyses were performed with the
STATISTICA v.7.1 package (StatSoft) and [R]
(http://www.r-project.org).
Results
Feeding behaviour
Feeding Preference experiments. In three out of the
four species comparisons conducted the native seagrass P. oceanica was preferred to the invasive
species. However, in the case of C. racemosa, this
species was significantly preferred to the native
seagrass (Fig. 1).
No-choice experiments. No choice experiments
mirrored the pattern observed in the feeding preference assays, as the invasive alga was consumed more
(96.1 ± 2.4 SE, %) than the native seagrass (63.0 ±
3.2 SE %, Table 1).
Impacts on herbivores
After ca. 10 weeks of running the experiment, all
urchins of both treatments from one tank died for
unknown reasons. Therefore, results presented below
are for to the urchins that were removed after 3 months
from other tanks and for which no mortality occurred.
When fed the native seagrass, sea urchins were
bigger (Table 2) and tended to have larger (but not
statistically significant) gonads and feeding apparatus
than sea urchins feeding on the invasive algae, which
had values of Test size, GI and LI similar to those of
the initial population (Fig. 2).
Plant traits and nutrient incorporation
Organic matter content (as % of DW), %C, and C/N
all differed significantly between species (Fig. 3a),
with all being highest for the native seagrass
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F. Tomas et al.
% Biomass Consumed
100
n = 13
z = 3.18
p = 0.002
80
n = 17
z = 2.53
p = 0.011
60
40
20
0
Lophocladia lallemandii
Posidonia oceanica
Acrothamnion preissii
Posidonia oceanica
% Biomass Consumed
100
n = 18
z = 3.593
p < 0.001
80
n= 5
z = 2.023
p = 0.043
60
40
20
0
Caulerpa racemosa
Posidonia oceanica
Womersleyella setacea
Posidonia oceanica
Fig. 1 Results of paired feeding preference experiments
between an introduced macroalgae (black) and the native
macrophyte Posidonia oceanica (white). Data are means
(?SE). Number of replicates (n), probability values (P) and
z statistics from Wilcoxon signed-ranks paired test are shown
Table 1 Repeated measures ANOVA performed to assess
differences in the consumption rates (%) among diets over the
time course of the experiment
Table 2 One-Way ANOVAs assessing the effects of diet
(native vs. invasive species) on sea urchin performance
parameters: growth (Test Diameter), reproductive output
(Gonadal Index) and feeding apparatus (LI)
df
MS
F
P
42.385
0.022
df
Species
1
14300.8
Error
2
337.4
Time
12
273.4
T9S
12
331.3
Error
24
99.9
2.736
P
4.994
0.042
3.315
0.40363
0.535
2.456
0.138
0.209*
Diet
1
85.56
0.175*
Error
14
17.13
Corrected after Greenhouse-Geisser adjustment
(P. oceanica) and lowest for the invasive alga
L. lallemandii (Fig. 3b, d). On the other hand there
were no significant differences in terms of N content
between the three species (Fig. 3c).
Repeated Measures ANOVAs revealed that sea
urchins fed native seagrass ingested significantly
higher quantities of organic matter, carbon and
nitrogen than those feeding on the invasive
C. racemosa (Table 3, Fig. 4).
123
F
Variable: Test diameter
Between-subjects sources of variation are the experimental
condition (invasive vs. native species) and within-subject
sources are Time (T) and interactions. df degrees of freedom,
MS mean squares
*
MS
Variable: GI
Diet
1
1.5610
Error
15
Variable: LI
3.8673
Diet
1
1.1603
Error
15
0.4725
df Degrees of freedom, MS mean squares
Discussion
Generalist herbivores are pre-adapted to feed on a
wide variety of plants (see Bernays and Minkenberg
1997) and can often expand their food range to
include new species. A recent meta-analysis on more
than 100 terrestrial and freshwater invasive species
Effects of invasive seaweeds on feeding preference and performance
b
Size
5,0
Reproduction
5,6
Feeding apparatus
4,5
a
50
5,2
4,0
LI (%)
55
GI (%)
3,5
4,8
3,0
4,4
2,5
45
Initial
C. racemosa
Initial
P. oceanica
Fig. 2 Performance parameters of sea urchins from the initial
population and of experimental sea urchins feeding on the
invasive species Caulerpa racemosa or the native seagrass
Organic Matter (% DW)
100
C. racemosa
P. oceanica
Initial
(A) F(2,6) = 8.422; p = 0.018
50
b
P. oceanica
(B) F(2,6) = 60.313; p < 0.001
a
b
80
a
60
40
20
40
a
30
c
20
10
0
0
C. racemosa
2,5
C. racemosa
Posidonia oceanica. Different letters indicate significant
differences between experimental treatments (SNK)
Carbon (% DW)
Test Diameter (mm)
60
P. oceanica
L. lallemandii
C. racemosa
35
(C) F(2,6) = 0.483; p = 0.639
P. oceanica
L. lallemandii
(D) F(2,6) = 12.759; p = 0.007
b
30
2,0
C/N
N (% DW)
25
1,5
1,0
a
20
15
a
10
0,5
5
0
0,0
C. racemosa
P. oceanica
L. lallemandii
C. racemosa
P. oceanica
L. lallemandii
Fig. 3 Nutritional traits for the native seagrass Posidonia
oceanica (white) and invasive species (black): a organic
matter, b carbon c nitrogen, and d C/N. Results of One-Way
ANOVA are presented (f, degrees of freedom, P value). Letters
represent significant differences between groups (SNK)
revealed that generalist native herbivores can incorporate exotic plants into their diet. This feeding
behavior contributes to suppressing the spread of
exotics (Parker et al. 2006) and provides biotic
resistance to native communities (Elton 1958). However, our results suggest that sea urchins are unlikely
to contribute to invasion control in the Western
Mediterranean, since the invasive seaweeds studied
are generally avoided or can potentially escape by
reducing herbivore performance. In fact, marine
generalist herbivores appear to globally avoid invasive seaweeds (see for e.g., Boudouresque et al. 1996;
Gollan and Wright 2006 for Caulerpa taxifolia;
Scheibling and Anthony 2001; Scheibling et al. 2008
for Codium fragile spp. tomentosoides, or Monteiro
et al. 2009 for Sargassum muticum), although juvenile stages of some invasive algae can be consumed
and suppressed (e.g., Thornber et al. 2004 for
Undaria pinnatifida, Sjotun et al. 2007 for Sargassum
muticum).
Although gut content analysis only allows for an
indirect snapshot of feeding behaviour, the absence of
several exotic species (i.e., L. lallemandii, W. setacea
and A. preissii) from P. lividus guts suggests that sea
123
F. Tomas et al.
Table 3 Repeated measures ANOVA performed to assess
differences in nutrient ingestion rates among diets
df
MS
F
P
27.568
0.034
Variable: Organic matter
Species
1
0.084
Error
2
0.003
Time
12
0.002
4.157
0.171
T9S
12
0.001
1.887
0.300
Error
24
0.001
33.457
0.029
Variable: Carbon
Species
1
0.021
Error
2
0.001
Time
12
0.000
3.951
0.180*
T9S
12
0.000
1.912
0.299*
Error
24
0.000
Variable: Nitrogen
Species
1
0.000
23.838
0.039
Error
Time
2
12
0.000
0.000
4.302
0.166*
T9S
12
0.000
1.877
0.301*
Error
24
0.000
Between-subjects sources of variation are the experimental
condition (invasive vs. native species) and within-subject
sources are Time (T) and interactions. df degrees of freedom;
MS: mean squares
*
Corrected after Greenhouse-Geisser adjustment
urchins do not incorporate these invasive seaweeds
into their diets (Ruitton et al. 2006; Cebrian et al. in
press). Our experiments support these results by
providing direct evidence that invaders are highly
avoided by sea urchins and escape enemy control by
reduction of herbivore preference. On the other hand,
C. racemosa is highly consumed in our preference
experiments, corroborating active feeding results from
gut content and caging experiments (Ruitton et al.
2006, Bulleri et al. 2009; Cebrian et al. in press).
We found no apparent relationship between feeding choices and nutritional characteristics of the
different species, suggesting that reduction of feeding
preference is not driven by nutritional quality (e.g.,
Cruz-Rivera and Hay 2001). Chemical defences often
deter sea urchins (e.g., Vadas 1977), and P. lividus is
sensitive to both chemical and structural defences of
Posidonia oceanica (Vergés et al. 2007a, b). Given
that seagrass blades are tougher than the thin
filamentous thallii of L. lallemandii, W. setacea and
A. preissii, differences in feeding behaviour are likely
driven by chemical characteristics. Lophocladia species produce alkaloids with cytotoxic effects (Gross
et al. 2006), which could act as a defense mechanism
against herbivores, but the presence of secondary
metabolites in W. setacea and A. preissii is unknown.
However, the highest diversity of secondary metabolites is found among rodophytes, and algae from the
family Rhodomelacea (which includes Womersleyella spp.) are particularly rich in halogenated compounds (Paul et al. 2001). Therefore, it is probable
that these two filamentous turf-forming species are
also chemically defended against herbivores.
Similarly, Caulerpa species produce caulerpenyne
(CYN), a secondary metabolite which is associated
with herbivore defence (Paul et al. 2007). Indeed, part
of the invasive success of C. taxifolia has been
attributed to the deterrent properties of CYN on
herbivores (Paul et al. 2007). Therefore, the strong
preference we observed for C. racemosa was unexpected. Nevertheless, the concentrations of CYN in
C. racemosa are much lower than in C. taxifolia
(Dumay et al. 2002, Box et al. 2010) and may be
tolerated by P. lividus. Furthermore, the presence of
the native Caulerpa prolifera in the Mediterranean
120
80
40
0
Carbon
Nitrogen
Ingestion ( mg d -1 ind -1)
Organic Matter
Ingestion ( mg d -1 ind -1)
Ingestion ( mg d -1 ind -1)
80
160
60
40
20
0
Caulerpa racemosa
Posidonia oceanica
3
2
1
0
Caulerpa racemosa
Posidonia oceanica
Caulerpa racemosa
Posidonia oceanica
Fig. 4 Ingestion of nutrients (organic matter, carbon and nitrogen) by sea urchins fed Posidonia oceanica (native seagrass, white) or
Caulerpa racemosa (invasive alga, black)
123
Effects of invasive seaweeds on feeding preference and performance
may have allowed the evolution of adaptations to
detoxify or tolerate certain levels of this metabolite
(Cornell and Hawkins 2003), making the congeneric
C. racemosa more susceptible to herbivores than
other exotics, which lack closely related species in
the novel range (Ricciardi and Ward 2006). However,
the specific defence mechanisms may differ among
Caulerpa species and types of herbivores, as suggested by the diverse responses of herbivores to the
different chemical extracts produced by Caulerpa
spp. (Davis et al. 2005).
Even though we found that C. racemosa is
preferred and largely consumed by sea urchins (see
also Bulleri et al. 2009; Cebrian et al. in press), it can
have negative effects on their performance. Such
effects are likely to result both from inadequate
nourishment levels (e.g., Berner et al. 2005), as well
as toxicity effects of seaweed chemical defences
(Targett and Arnold 2001; Box et al. 2009). Our study
shows that sea urchins exhibited compensatory
feeding in the no choice experiments, which is a
common adaptive response of herbivores when faced
with low quality food (e.g., Cruz-Rivera and Hay
2000; Berner et al. 2005). However, such compensatory feeding of C. racemosa was not enough to
provide higher inputs of organic matter, carbon and
nitrogen than those provided by the native seagrass,
with negative consequences on herbivore performance (e.g., Fink and Von Elert 2006). In the field,
where other food is available, diet mixing could be a
strategy that generalist herbivores employ to avoid
unbalanced nutrition and diminish toxicity effects of
a particular species (e.g., Cruz-Rivera and Hay 2000;
Moreau et al. 2003; Box et al. 2009).
The high consumption of C. racemosa would
initially suggest a certain capacity of herbivores to
provide biotic resistance to native communities.
However, the results that herbivore performance is
diminished when fed C. racemosa run counter this
idea. In fact, herbivore escape may be enhanced and
sea urchins may need to incorporate alternative food
sources to maintain nutritional requirements, limiting
their capacity to suppress the spread of C. racemosa
(e.g., Bulleri et al. 2009; Cebrian et al. in press). In
addition, the high growth and reproduction capacities
of C. racemosa (e.g., Piazzi and Cinelli 1999;
Panayotidis and Žuljević 2001) could also compensate for biomass loss by herbivory, contributing to
invasion success. In invaded seagrass meadows,
however, the availability of alternative native food
sources other than P. oceanica blades can be very
restricted (Piazzi and Cinelli 2001; OcchipintiAmbrogi and Savini 2003; Ballesteros et al. 2007,
personal observation). In such cases preferential
feeding on seagrass by native herbivores may further
facilitate seaweed invasions by indirectly enhancing
the competitive abilities of exotic algae.
Experiments on sea urchin performance lasted
3 months and allowed the detection of adverse effects
on growth. Food limitation in sea urchins commonly
causes reduction or inversion (i.e., shrinking) in
growth rate (e.g., Levitan 1988; Edwards and Ebert
1991), reduced reproductive output, and changes in
the size of feeding apparatus (e.g., Fernandez and
Boudouresque 1997). The feeding apparatus and the
reproductive output tended to be smaller in urchins
feeding on C. racemosa than on those feeding on the
native species, and would have likely become
significantly smaller in a longer-term experiment
(e.g., Tomas et al. 2005b; Lyons and Scheibling
2007). High plasticity in sea urchins probably allows
survival of individuals in the short term but may
increase susceptibility to predators (e.g., Sala and
Zabala 1996) or decrease larval production and
performance (e.g., George 1996), which may carry
important long-term ecological consequences at the
population level. These could be particularly relevant
for such generalist herbivores that are key interactors
in subtidal benthic ecosystems. In addition, given the
significant commercial interest of sea urchins
(Lawrence 2001), impacts on their populations could
have further negative economic consequences.
Furthermore, assessing the impacts of consuming
C. racemosa on the performance of a native herbivore
has allowed the identification of an enemy escape
mechanism, and helps solve the apparent paradox
raised between high preference and consumption of
C. racemosa and the inability of sea urchins to limit
its spread (Bulleri et al. 2009; Cebrian et al. in press).
Finally, examining the impacts of invasive taxa on
the fitness of native species is essential for recognizing the full ecological effects of invasive species
(e.g., Wright and Gribben 2008, Tallamy et al. 2010),
and is particularly relevant for species with strong
ecological and economic roles such as sea urchins.
Acknowledgments The authors are indebted to R. Gradel
and the ‘‘Palma Aquàrium’’ staff for providing facilities and
123
F. Tomas et al.
invaluable assistance with the experiments. We would also like
to thank E. Ballesteros, A. Ceballos, N. Comalada, E. Infantes,
F.J. Medina, A. Sureda, and S. Deudero and her students for
help in the field and the laboratory, as well as P. Fernandez
from the ‘‘Serveis Cientı́fico Tècnics’’ University of Barcelona
for assistance with C/N analyses. Financial support was
provided by Grant CTM2005-01434/MAR from the Spanish
Ministry of Science and Innovation. FT was funded by Juan de
la Cierva Postdoctoral Fellowship.
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