Distribution and population dynamics of the introduced seaweed Grateloupiaturuturu (Halymeniaceae, Rhodophyta) along the Portuguese coast

RITA ARAUJO1*, JOSE VIOLANTE

1, RUI PEREIRA1, HELENA ABREU

1, FRANCISCO ARENAS1

AND ISABEL SOUSA-PINTO1,2

1CIMAR/CIIMAR – Interdisciplinary Centre for Marine and Environmental Research, University of Porto, Rua dos Bragas,

289, 4050-123 Porto, Portugal2Department of Botany, Faculty of Sciences, University of Porto, Rua do Campo Alegre, Porto, Portugal

ARAUJO R., VIOLANTE J., PEREIRA R., ABREU H., ARENAS F. AND SOUSA-PINTO I. 2011. Distribution and populationdynamics of the introduced seaweed Grateloupia turuturu (Halymeniaceae, Rhodophyta) along the Portuguese coast.Phycologia 50: 392–402. DOI: 10.2216/10-65.1

Despite the increasing number of coastal areas invaded over the last years by the introduced seaweed Grateloupia

turuturu, studies on this species are scarce worldwide, and its invasive capability and future impacts remain unexplored.In the present study, we describe the geographical distribution of the species after a few years of colonization of thePortuguese continental coastline. Additionally, we examine the structure and dynamics of one of the first population ofGrateloupia in our shores. Seasonal dynamics of standing biomass, density, size structure and inequality (sizevariability), together with the presence of fertile fronds were investigated during one year. Grateloupia was recorded inmidintertidal pools at 11 of the 36 localities sampled, two of which presenting an elevated abundance of fronds. Frondswere present during the entire year, but their size (length and biomass), density and size inequality varied seasonallyreaching highest values at the beginning of the summer. The annual cycle of the population studied included a slow-growth phase in winter, a fast-growth phase during spring-early summer when some density-dependent regulationappeared to occur, as well as a dieback phase at the end of summer. In terms of fertility, abundance of fronds bearingreproductive structures were seasonally variable although carposporophytic and tetrasporophytic fronds were recordedthroughout the year. The results of this work highlight some of the biological characteristics of Grateloupia turuturu thatmay determine its invasive nature and its possible impact on native ecosystems.

KEY WORDS: Geographical distribution, Grateloupia turuturu, Introduced species, Macroalgae, Population dynamics,Portugal

INTRODUCTION

Introductions of nonindigenous species are globally con-

sidered a threat to marine biodiversity, seriously impacting

native ecosystems worldwide (Carlton & Geller 1993; Bax et

al. 2001). In the European seas, more than 800 introduced

species have been reported, mostly in coastal areas

(Streftaris et al. 2005). Marine macroalgae are a significant

component of these introduced marine species, including

several highly prominent species that have caused signifi-

cant ecological and economic impact: e.g. Caulerpa taxifolia

(M. Vahl) C. Agardh, Codium fragile (Suringar) Hariot,

Sargassum muticum (Yendo) Fensholt or Undaria pinnati-

fida (Harvey) Suringar (Schaffelke et al. 2006). For most of

these introduced species there is insufficient information on

their current status and ecology in their new habitats,

preventing the prediction of their future impacts and

adoption of management politics.

The Portuguese coast is not as heavily invaded as other

European shores, and only 11 introduced species have been

recorded in this area (Araujo et al. 2009): Anotrichium

furcellatum (J. Agardh) Baldock, Antithamnionella spiro-

graphidis (Schiffner) E.M. Wollaston, Antithamnionella

ternifolia (J.D. Hooker & Harvey) Lyle, Antithamnion

densum (Suhr) M.A. Howe, Asparagopsis armata (Harvey)

[‘‘Falkenbergia rufolanosa’’ stage (Harvey) F. Schmitz],

Dasya sessilis Yamada, Grateloupia turuturu Yamada,

Gracilaria vermiculophyla (Ohmi) Papenfuss, Neosiphonia

harveyi (J. Bailey) M.-S. Kim, H.-G. Choi, Guiry & G.W.

Saunders, Sargassum muticum and Undaria pinnatifida.

Although the majority of these species were reported at low

local abundances for a few locations, some of them, e.g.

Antithamnionella ternifolia, Grateloupia turuturu and Sar-

gassum muticum, are widely spread along the Portuguese

coast (Araujo et al. 2009). Grateloupia turuturu, a recent

introduction to the Portuguese shores (Araujo et al. 2003),

is quickly becoming more abundant, and despite being

reported worldwide as an invasive species (Villalard-

Bohnsack & Harlin 1997; Verlaque et al. 2005), it is still

poorly studied.

Grateloupia turuturu is native to Japan and has been

reported on the Atlantic coasts of Europe and North

America and in the Mediterranean Sea (Cabioch et al. 1997;

Villalard-Bohnsack & Harlin 1997; Barbara & Cremades

2004). More recently it has been recorded in Australia

(Saunders & Withall 2006) and New Zealand (D’Archino et

al. 2007). Studies developed in France (Cabioch et al. 1997;

Simon et al. 2001), England (Cabioch et al. 1997) and the

United States (Harlin & Villalard-Bohnsack 2001; Villa-

lard-Bohnsack & Harlin 2001) had identified this species as

G. doryphora. However, Gavio & Fredericq (2002) using

comparative morphology and molecular analysis, showed* Corresponding author (ritaraujo@ciimar.up.pt).

Phycologia (2011) Volume 50 (4), 392–402 Published 13 July 2011

392

that these previous works refer to misidentified specimens

of G. turuturu.

Grateloupia turuturu grows in both sheltered and exposed

areas (Villalard-Bohnsack & Harlin 1997; Simon et al.

2001), can tolerate wide variations of temperature and

salinity (Simon et al. 1999; Harlin & Villalard-Bohnsack

2001) and is well adapted to eutrophic conditions (Simon et

al. 2001). This species shows multiple recruitment strategies

(Harlin & Villalard-Bohnsack 2001) and fertile individuals

occur throughout the year in some locations (Harlin &

Villalard-Bohnsack 2001; Simon et al. 2001; Villalard-

Bohnsack & Harlin 2001).

The sources of introduction of this species are still not

clearly established although some evidence exists relating

Grateloupia turuturu’s introduction with aquaculture activ-

ities (in particular oyster farming), ship fouling and

ballasting (Villalard-Bohnsack & Harlin 1997) and short-

distance dispersal by stone-rafting and drifting of fertile

blades (Simon et al. 1999; Simon et al. 2001).

Whereas a large amount of literature exists reporting

invasions by some marine macroalgal species like Sargas-

sum muticum (Arenas & Fernandez 2000; Staehr et al. 2000;

Plouguerne et al. 2006; Engelen & Santos 2009) or Caulerpa

taxifolia and Caulerpa racemosa (Piazzi et al. 2001; Balata

et al. 2004), studies on Grateloupia turuturu are insufficient

(Harlin & Villalard-Bohnsack 2001) despite its recently

noticed expansion range (D’Archino et al. 2007; Mathieson

et al. 2008) and its possible invasive nature (Villalard-

Bohnsack & Harlin 1997; Verlaque et al. 2005).

The overall impact of introduced species is directly linked

both with their final range of expansion and their local

abundances in the host communities (Parker et al. 1999).

To increase our capabilities for prediction of both the

spread and invasive nature of introduced species, detailed

and relevant information on the ecology of the species in its

new range of distribution is imperative. Moreover, this is

basic information for the implementation of preventive and

management actions.

The objectives of this work were to assess the current

geographical range of Grateloupia turuturu on the Portu-

guese coast and to investigate the structure and dynamics

(reflected in the seasonal variations of population param-

eters), including the different life-cycle phases, of the most

established population of this species in our shores. We

specifically studied the existence of temporal and small-

scale spatial variability in the frond length, biomass,

density, size distribution and size inequality of fronds. We

also examined the existence of significant temporal and

spatial differences in the reproductive status and relative

dominance of life-cycle phases in the population studied.

The biological characteristics of an introduced species are

important predictors of its invasive nature and consequent

impact in native communities.

MATERIAL AND METHODS

Study area

The study of the geographical distribution of Grateloupia

turuturu was conducted in the northern Portuguese coast

(Fig. 1). In this area the tidal regime is semidiurnal,

reaching 3.5–4 m, during spring tides and sea surface

temperature varies between 13 and 20uC during the year.

The study of the structure and dynamics of G. turuturu

populations was performed in rock pools situated in the

midintertidal level, shallower than 1 m and with size

between 1 m2 and 5 m2. Organisms living in these systems

experience unique fluctuations of environmental parame-

ters. Although environmental variations in rock pools are

already documented (Metaxas & Scheibling 1993), a brief

characterization of the environmental parameters fluctua-

tions experienced during low tide in rock pools of the

studied area was performed. From December 2008 to

November 2009, the temperature in one G. turuturu

dominated rock pool was registered hourly using data

loggers (Stow Away Tidbit Temp Logger). Mean annual

temperature was 16.07uC, ranging from a minimum of

8.2uC and a maximum of 28.62uC. Additionally, in three

different dates of sampling (June, August and November),

temperature, salinity and light (under and above canopy)

were registered hourly during the period of low tide in three

of the G. turuturu dominated rock pools (at each hour five

measures were done for salinity and temperature and 10

measures for light under and above canopy). Mean

temperature during low tide was 20uC with maximum

values of 28.9uC and minimum values of 13.7uC. During the

summer (August) temperature amplitude in pools during

low tide reached 7uC, whereas in winter (November)

temperature fluctuations were of 3uC. Mean salinity was

33.82%, with maximum values of 36.7% and minimum

values of 20% (during rainy days). Mean light below

canopy was 45.65 meinstein/m2 (mM), fluctuating between

273 mM and 0.6 mM, while above canopy a mean of

404.16 mM was registered, with maximum values of 886 mM

and minimum values of 15 mM. Light penetration was

reduced in November when compared with August. Mean

values registered above canopy were 760 mM in summer

and 229.03 mM in winter, while under canopy mean light

intensity was 75.67 mM in summer and 42.63 mM in winter.

Geographical distribution

To assess the geographical distribution of Grateloupia

turuturu on the Portuguese coast, 36 sites (all the

independent areas of the rocky shore) along a stretch of

250 km of the northern shore were visited from 2000 to

2007: sites with sparse distribution of fronds were visited

from May to September, but sites with well established

populations were visited at least once in each different

month (Fig. 1). This study was not extended further south

because the species was never reported at any other locality

further than our southernmost sampling locality (Buarcos)

(E. Berecibar, personal communication), with the exception

of a citation by L. Pereira (personal communication) in

Peniche (Fig. 1). At each locality, the intertidal area, from

high to low littoral (until 21 m mean low water), was

thoroughly surveyed (the shore was covered by foot and

visually surveyed) and G. turuturu specimens collected

whenever present. An evaluation of the abundance of

fronds at each site was done, distinguishing places with a

scarce distribution of fronds from localities with well

Araujo et al.: Geographical distribution and population dynamics of Grateloupia turuturu on the Portuguese coast 393

established populations. The relationship between popula-

tions density and distance from major ports was estimated

using the nonparametric Spearman correlation index.

Population structure and dynamics

The structure and dynamics of a population of Grateloupia

turuturu was studied at the most established population

(with higher abundance of fronds), located in Aguda

(41u039250N; 8u399240W). At this locality G. turuturu was

mainly found in intertidal rock pools.

From September 2004 to July 2005, population descrip-

tors such as frond length, biomass, density and size

distribution of fronds were studied bimonthly in three

randomly selected pools. Care was taken to avoid sampling

the same pool twice. In each pool, two 50 3 50 cm quadrats

were randomly chosen and destructively sampled. All the

Grateloupia turuturu specimens inside each quadrat were

scrapped, bagged and preserved in 4% formalin seawater.

In the laboratory, all the fronds collected were counted and

their length measured. Fronds biomass of G. turuturu was

estimated from a length-biomass relationship obtained by

measuring total length and dry weight of each of 127

fronds, collected between March and July. Fronds were

dried in an oven at 50uC for 48 h. The Gini coefficient (G)

was the size-structure descriptor selected for this study

(Bendel et al. 1989). This coefficient has been used in several

studies to describe the total amount of inequality in size of

plant populations (Santos 1995; Arenas & Fernandez 2000;

Damgaard & Weiner 2000). The coefficient ranges from a

minimum value of zero (when all the individuals have the

same size) to a theoretical maximum of one (when all

individuals except one have a size of zero) (Weiner &

Solbrig 1984).

Fig. 1. Study area with the sampling localities marked with numbers. Geographical distribution of Grateloupia turuturu is signalized withbold numbers and dot symbols filled in grey. The year G. turuturu was first observed in each location is included in brackets and theabundance of each population indicated. 1 – Insua de Caminha; 2 – Moledo; 3 – Vila Praia de Ancora; 4 – Forte do Cao; 5 – Montedor; 6 –Areosa; 7 – Viana do Castelo; 8 – Lima’s saltmarsh; 9 – Amorosa; 10 – Castelo do Neiva; 11 – Belinho; 12 – S. Bartolomeu do Mar; 13 – Riode Moinhos; 14 – Cepaes; 15 – Esposende; 16 – Cavado’s saltmarsh; 17 – Apulia; 18 – Agucadoura; 19 – Quiao; 20 – Povoa do Varzim; 21 –Vila do Conde; 22 – Mindelo; 23 – Praia dos Electricos; 24 – Angeiras; 25 – Cabo do Mundo; 26 – Leca da Palmeira; 27 – Foz do Douro;28 – Lavadores; 29 – Valadares; 30 – S. Felix da Marinha; 31 – Miramar; 32 – Aguda; 33 – Espinho; 34 – Ria de Aveiro; 35 – Barra deAveiro; 36 – Buarcos. The occurrence of the species in Peniche (L. Pereira, personal communication) is signalled. Main ports of the northernPortuguese coast are represented.

394 Phycologia, Vol. 50 (4), 2011

To test the existence of temporal and small-scale spatial

variability in the population descriptors studied, univariate

analysis of variance (two-way ANOVA) was performed.

The assumption of homogeneity of variances was tested

using Cochran’s test and, when appropriate, data transfor-

mation was performed (Underwood 1997). Analysis in-

cluded two factors: Time (fixed, with six levels correspond-

ing to each sampling date) and Pool (random, with three

levels).

Reproduction

Grateloupia turuturu exhibits a haploid-diploid life cycle,

including two independent isomorphic reproductive phases

[tetrasporophyte (diploid) and gametophyte (haploid)] and

a third reproductive stage (carposporophyte), developed

within the female gametophyte.

To study the reproductive dynamics of Grateloupia

turuturu, the reproductive status of all the fronds collected

in the 50 3 50 cm plots was determined for all the sampling

occasions. All the new fronds below 5 cm were considered

recruits, but fronds smaller than 5 cm growing from older

damaged fronds were not included in this category.

However, this study was unable to distinguish between

fronds formed from new and old crusts. Female gameto-

phytes/carposporophytes were identified by naked eye,

whenever the fronds were obviously mature. In the case

of tetrasporophytic fronds or when the identification of the

reproductive status was not obvious, cross-sections of the

blade were observed under a dissecting microscope. To test

for temporal and small-scale spatial significant variations in

the reproductive status (number of reproductive and

nonreproductive fronds) and in the life-cycle phase (number

of carposporophytic and tetrasporophytic fronds), univar-

iate analysis of variance (three-way ANOVA) was per-

formed. The assumption of homogeneity of variances was

tested using Cochran’s test and, when appropriate, data

transformation was performed (Underwood 1997). Analy-

sis included three factors: Reproductive status or Life-cycle

phase (fixed, with two levels), Time (fixed, with six levels

corresponding to each sampling date) and Pool (random,

with three levels). Student – Newman – Keuls (SNK) tests

were used for a posteriori comparisons of means. ANOVA

was performed using the GMAV5 software (University of

Sydney).

RESULTS

Geographical distribution

On the Portuguese coast, Grateloupia turuturu occurs

mainly in midintertidal rock pools of both sheltered and

exposed rocky shores, although, in some locations, it was

also found at the low littoral level. G. turuturu was found at

11 of the 36 surveyed localities (Fig. 1). At two of these

localities [Aguda (32) and Foz do Douro (27)] this species

presented elevated abundances (. 25% of percentage cover)

in midintertidal pools. In one locality [Buarcos (36)] the

species was present at intermediate abundances (5–25% of

percentage cover), and at all the other localities sampled,

fronds were sparsely distributed along the shore (, 5% of

percentage cover). The geographical distribution of G.

turuturu on the Portuguese coast was not continuous along

the rocky shore, although suitable substratum (rocky shore)

for its establishment was available along the surveyed

coastline. Instead, G. turuturu populations were mainly

found nearby the main shipping ports of the northern coast

of Portugal (Fig. 1). However, the distance from main ports

(port of Viana do Castelo, port of Leixoes, port of Aveiro

and port of Figueira da Foz) was not significantly

correlated with the density of G. turuturu populations

(Table 1).

Population structure and dynamics

Grateloupia turuturu’s fronds showed a wide variety of

morphological forms from lanceolate (simple or divided) to

fronds with marginal proliferations (Figs 2–5). Blade size

varied seasonally with maximum blade length (72 cm) in

May and July. Frond length was much lower at all the

sampling dates, varying from a minimum of 2.03 cm 6 0.06

(mean 6 SE) in March to a maximum of 10.99 cm 6 0.34

(mean 6 SE) in September. Length and biomass were

positively correlated for G. turuturu fronds and biomass

was calculated, for each frond, based on the following

equation: Ln B 5 27.6206 + 1.9072*Ln L (r 5 0.937, P ,

0.001), where B is frond biomass and L is frond length (N 5

127). Except for the first sampling date, September, the

studied population was dominated by fronds of small size

(length , 5 cm) (Fig. 6). This dominance was stronger

between March and July when the percentage of small

fronds averaged 82.16% 6 5.96. During this period the

largest fronds (. 10 cm) were also recorded, representing

around 8% of the population fronds. All the population

descriptors studied differed significantly among sampling

dates (Table 2), and in the case of mean frond length, pool

was also a significant factor (Table 2). No significant

interactions Time 3 Pool were found for any of the

variables studied (Table 2). The annual cycle of the G.

turuturu population studied included different development

phases. During winter (November–March), no significant

changes in biomass, density and Gini coefficient were

recorded (Fig. 7). Minimum values of standing biomass

(1.56 6 0.4 g/m2), density (640 6 141.18 fronds/m2) and

Gini coefficient (0.35 6 0.02) were recorded during this

period (Fig. 7). From March to early summer, a growth

period occurred with significant increases in biomass and

size inequalities. No significant differences were found for

plant density among dates (probably due to the high

variability among quadrats), but the number of plants

Table 1. Spearman correlation between the distance from mainports and population density (Pden) in each of the localitiessampled.

Valid Spearman T (N 2 2) P

Port Viana do Castelo& Pden 11 0.526091 1.85586 0.096448

Port Leixoes & Pden 11 20.104062 20.31389 0.760758Port Aveiro & Pden 11 20.460655 21.55700 0.153896Port Figueira da Foz

& Pden 11 20.526091 21.85586 0.096448

Araujo et al.: Geographical distribution and population dynamics of Grateloupia turuturu on the Portuguese coast 395

progressively increased until May when the maximum

densities were found (maximum mean density 2182.7 6

1126.41 fronds/m2, with a single plot maximum of 7692

fronds/m2). Maximum mean standing biomass was found in

July (13 6 1.46 g/m2), when some of the other population

descriptors like density and size inequality appeared to be

already declining (Fig. 7). Later in the summer (September)

the population was maintained by few old big fronds

(Fig. 6). During this period minimum values of density and

Gini coefficient were recorded simultaneously with low

levels of standing biomass (Fig. 7).

Reproduction

Fronds with reproductive structures were found throughout

the year and were dominant among those larger than 5 cm

long, except for March and May when no significant

differences were found between the number of reproductive

and nonreproductive fronds (Fig. 8) (Table 3). Neverthe-

less, two reproductive peaks were recorded: one in winter

(January) and another one at the beginning of the summer

(July) (Fig. 8). These peaks of abundance of reproductive

fronds were not coincident with the peaks of incorporation

of smallest size individuals (presumably new recruits) into

the population (Figs 6, 8). Mature tetrasporophytes and

female gametophytes/carposporophytes were recorded at

all sampling dates (Fig. 9), but male gametophytes were

never found throughout the study. Carposporophytic

fronds outnumbered the tetrasporophytic ones at all dates,

except for September, March and July (Fig. 9) (Table 4).

DISCUSSION

In this study Grateloupia turuturu was found in 30% of the

visited localities (11 out of 36), occupying rocky shores

along a 200 km stretch of the Portuguese coast. Dispersal of

G. turuturu to new locations occurs by two main processes:

(1) primary remote dispersal events often favoured by

human activities and characterized by spatial discontinuity

between donor and new established population and (2)

secondary marginal dispersal events to adjacent locations

(Simon et al. 2001). The geographical distribution of the

Portuguese populations, grouped around the main com-

mercial harbours in the area (Viana do Castelo, Leixoes,

Aveiro, Figueira da Foz and Peniche) and separated by 10s

of kms, suggest the occurrence of both primary and

secondary dispersal modes. Shipping related activities

would originate founder populations from where G.

turuturu would disperse into neighbour suitable localities.

The dispersal capability of G. turuturu is unknown but it

seems to be able to establish new populations and spread

along the shoreline in relative short periods of time.

However, the lack of a significant correlation between the

distance from main ports and the density of G. turuturu

populations suggests that other factors than the dispersal

characteristics of the species might account for the

geographical patterns found. The establishment of an

introduced species in a new environment is also dependent

on the interactive effects of factors like the environmental

and biological conditions encountered at the recipient

community and the biological traits of the introduced

species (Romanuk & Kolasa 2005; Beisner et al. 2006).

Invasive seaweeds commonly exhibit a group of charac-

teristics that confer them opportunistic, stress tolerant and/

or biological competent capabilities and consequent capa-

bility for invasiveness (Valentine et al. 2007). The estab-

lishment of an invasive species in native communities is

facilitated by the occurrence of disturbance events that

release space for new colonizers, but life history character-

istics of the invader are also determinant for its introduc-

tion and persistence in native communities (Valentine et al.

2007). The annual cycle of the population of Grateloupia

turuturu studied included two growing phases: a slow

growing winter phase, characterized by little changes in

mean length, standing biomass, density and size inequality

of fronds and a fast-growing spring phase, when the

population simultaneously increased its standing biomass,

Figs 2–5. Herbarium specimens collected along the Portuguesecoast.

Fig. 2. Specimen collected in Leca da Palmeira (August 2004;PO-Algae 3216).Fig. 3. Specimen collected in Foz do Douro (August 2004; PO-Algae 3213).Fig. 4. Specimen collected in Angeiras (October 2004; PO-Algae3220).Fig. 5. Specimen collected in Buarcos (July 2000; PO-Algae2336).

396 Phycologia, Vol. 50 (4), 2011

density and size inequality. These results highlight impor-

tant life history characteristics of G. turuturu that may

influence its invasive potential like the presence of blades

during the entire year with capability of increasing their

abundance even during the periods when environmental

conditions are unfavorable for the majority of the seaweed

species.

The seasonal pattern of abundance of Grateloupia

turuturu on the Portuguese coast was similar to that

described for Galicia (Barbara & Cremades 2004) and

Britanny (Cabioch et al. 1997; Simon et al. 2001).

Seasonality in macroalgae is controlled by several factors

like temperature, photoperiod, nutrient availability, com-

petition, grazing or by the combination of several of these

factors (Lobban & Harrison 1997). G. turuturu occurs on

the Portuguese coast mainly in mid and high intertidal rock

pools. These spatially variable habitats (Araujo et al. 2006)

experience pronounced fluctuations of environmental

factors (both daily and seasonal) when compared to those

permanently submerged (Metaxas & Scheibling 1993). In

the population studied, the period of senescence of blades

(from July to September) was coincident with the period of

the year when extreme temperature values are usually

recorded (in August the temperature of the water in rock

pools of the study area can reach 29uC with temperature

fluctuations during low tide of 7uC). Although G. turuturu

can grow under a wide range of salinity and temperature

conditions (Simon et al. 1999), temperature extremes,

rather than mean temperature values, may determine the

survival of G. turuturu blades (Harlin & Villalard-Bohnsack

2001).

Light availability may also play an important role in the

seasonal dynamics of the Grateloupia turuturu population

studied. When plants are growing in crowded conditions,

light might become the main limiting factor for survivor-

ship and growth (Schwinning & Weiner 1998). Under these

conditions self-thinning may occur, involving the disap-

pearance or growth suppression of small individuals, as a

result of asymmetric competition with larger plants (Weller

1987). Although in the past self-thinning was considered a

universal process, positive relationships between frond

density and biomass have also been reported for several

Fig. 6. Temporal variation in frond-length frequency distribution of Grateloupia turuturu fronds in the population studied.

Table 2. ANOVA testing the effects of sampling date and rock pool on mean length, wet standing biomass, density and size inequality.1

Source ofvariation df

Mean length Dry standing biomass Density Gini coefficient

MS F MS F MS F MS F

Date (Da) 5 1.9176 28.20*** 2.6618 4.94* 609.2037 3.45* 0.0814 16.54***Pool (Po) 2 0.2908 4.28* 0.2020 0.37 n.s. 73.8963 0.42 n.s. 0.0106 2.16 n.s.Da 3 Po 10 0.0680 0.43 n.s. 0.5387 1.38 n.s. 176.5809 0.53 n.s. 0.0049 0.59 n.s.Residuals 18 0.1579 0.3915 336.0118 0.0083

Cochran’s test C 5 0.33; n.s. C 5 0.42; n.s. C 5 0.30; n.s. C 5 0.17; n.s.Transformation Ln (x + 1) Ln (x + 1) Ln (x + 1) None

1 df, degrees of freedom; MS, mean squares; n.s., nonsignificant; *P , 0.05; ***P , 0.001.

Araujo et al.: Geographical distribution and population dynamics of Grateloupia turuturu on the Portuguese coast 397

seaweeds species (Santos 1995; Scrosati & DeWreede 1997;

Scrosati 2000). In the studied population, at the end of the

fast growing period, an increase in biomass was followed by

a decrease in density caused by the reduction in the number

of smaller blades. Size inequality also decreased because the

disappearance of small fronds (that were dominant in the

population) reduced the variability in frond size. These

findings are in agreement with density regulation by self-

thinning, when biomass and density were simultaneously at

their maximum although the decrease in the number of

small size blades can also be related with a diminishment in

the recruitment success. Interactions between species are

major structuring agents of seaweed communities (Chap-

man 1986), and in many cases disturbance events in native

assemblages create the opportunity for alien species to

establish at high densities (Valentine & Johnson 2003,

2004). G. turuturu was capable of simultaneously increase

its frond biomass and density without intraspecific regula-

tion, which might be determinant for its competitive

dominance when patches of bare space are available for

colonization.

Fronds of Grateloupia turuturu bearing reproductive

structures were found during the entire year but their

abundances varied seasonally. The relative abundance of

gametophytic and tetrasporophytic fronds is an important

descriptor of populations structure for seaweeds with

different life-history phases (Scrosati & Mudge 2004a).

Carposporophytic fronds were more abundant than tetra-

sporophytic fronds in three of the sampling occasions.

Similar patterns of gametophytic dominance were found for

other seaweed species (Scrosati & Mudge 2004a, b), but the

opposite trend of life-phase dominance was also described

for some species (Carmona & Santos 2006). In general,

Gigartinales seem to have a dominance of gametophytes

(Scrosati & Mudge 2004a, b; Thornber & Gaines 2004)

while tetrasporophytes are the most abundant life phase in

Fig. 7. Temporal variation in a) mean length (cm, mean 6 standard error, n 5 6), b) dry standing biomass (gm22, mean 6 standard error, n5 6), c) frond density (number fronds m22, mean 6 standard error, n 5 6) and d) frond size inequality (mean 6 standard error, n 5 6) forGrateloupia turuturu fronds in the population studied.

398 Phycologia, Vol. 50 (4), 2011

Gelidiales (Melo & Neushul 1993; Carmona & Santos

2006). For Cryptonemiales like G. turuturu these patterns of

dominance are not studied. The imbalance in the gameto-

phyte-tetrasporophyte ratio found in this study might be

related with different requirements of the two life phases

that enhance their abundance under particular conditions.

Distinct physiological responses between life phases were

described for different species for parameters like the

resistance to desiccation (Scrosati & Mudge 2004a),

mechanical properties (Carrington et al. 2001), density of

antifouling structures (Plouguerne et al. 2007), vegetative

growth rate and spore release (Carmona & Santos 2006)

and algal quality and production of defense compounds

(Verges et al. 2008). Recent works have shown that

fecundity and fertility of different life-cycle phases and the

interactive effects of environmental conditions can be

determinant for the gametophyte-tetrasporophyte ratio

found in seaweed populations (Thornber & Gaines 2004;

Fierst et al. 2005). For G. turuturu the ratio between

different life-history stages has not been studied elsewhere;

therefore we do not know the importance of this factor in

the invasive process.

In the population studied the periods of highest

abundances of reproductive fronds and of small size

individuals (presumably recruits) were not temporally

coincident. This decoupling could result from failures in

recruitment due to environmental conditions (e.g. UV

radiation and sedimentation) or grazing, both being also

seasonally variable (Diaz-Pulido & McCook 2003; Schiel et

al. 2006; Zacher et al. 2007; Navarro et al. 2008). Survival

of recruits might be enhanced by mild environmental

conditions experienced in spring and autumn and reduced

by extreme environmental conditions during summer and

winter. Additionally, seasonality might also affect the

reproductive potential of fertile blades. Seasonal differences

in relative fecundity, spore release and germination were

found for the tetrasporophytic phase of Gelidium robustum,

although reproductive fronds were present over the entire

year (Melo & Neushul 1993). The abundance of Grateloupia

turuturu’s recruits might also result from the use of other

recruitment strategies besides the formation of fronds by

spore germination. New fronds can also arise from older

crusts, from older damaged fronds and from new crusts

produced by older crusts or fronds (Harlin & Villalard-

Bohnsack 2001). The reproductive output and germination

Fig. 8. Temporal variation in the proportion of fronds (above 5 cm long) bearing reproductive structures in the population studied.

Table 3. ANOVA testing for significant differences in the numberof reproductive and nonreproductive fronds (reproductive status)between sampling dates and rock pools.1

Source ofvariation df MS F

Reproductivestatus (Rs)

1 154.448 246.68***

Date (Da) 5 2.303 1.62 n.s.Pool (Po) (Da) 12 1.4252 1.26 n.s.Rs 3 Da 5 4.9928 7.397**Rs 3 Po (Da) 12 0.6261 0.56 n.s.Residuals 36 1.1268

Cochran’s test C 5 0.2; n.s.Transformation Ln (x + 1)

SNK test Rs 3 DaN reproductive 5 N nonreproductivedate 4 (Mar.) and 5 (May)N reproductive . N nonreproductivedate 1 (Sep.), 2 (Nov.), 3 (Jan.) and 6 (Jul.)

1 df, degrees of freedom; MS, mean squares; n.s., nonsignificant;**P , 0.01; ***P , 0.001.

Araujo et al.: Geographical distribution and population dynamics of Grateloupia turuturu on the Portuguese coast 399

success of an introduced species are important predictors of

its invasiveness. Propagule pressure is a strong controlling

factor of the invasion process (Britton-Simmons & Abbott

2008) and the probability of successful invasions increases

with the number of propagules released, with the number of

introduction attempts and with introduction rate (Grevstad

1999; Ahlroth et al. 2003; Drake et al. 2005). The

reproductive potential of Grateloupia turuturu with fertile

fronds and new recruits during the entire year is consistent

with high potential for propagule pressure and indicates the

invasive nature of this species.

Grateloupia turuturu is rapidly spreading world-wide and

has been suggested to be invasive by several authors

(Villalard-Bohnsack & Harlin 2001; Nyberg & Valentinus

2005; Verlaque et al. 2005; Saunders & Withall 2006). The

results of our work provide new insights in the biology of

this species, highlighting its possible invasive nature in

native ecosystems. In particular: (1) the occurrence of

blades with reproductive structures (and recruits) during

the entire year show its availability to colonize gaps of free

space in an opportunistic way; (2) the species is able to

create very high density populations and the simultaneous

increase in biomass and density values until both maxima

are reached suggest an elevated capability of occupation of

space before intraspecific regulation occurs indicating its

inter-specific competitive potential; and (3) the increase in

the number of localities where the species has been found,

in the past 8 years, is a sign of its spreading abilities and

invasive potential. The data here presented show that G.

turuturu should be considered a potential threat for the

European coasts as well as worldwide for other regions with

similar environmental conditions. Further studies are

needed to accurately determine the structural and func-

tional impacts of this species in native communities.

However, based on the ecological characteristics of G.

turuturu highlighted in this study and on the previous

knowledge about the physiological tolerance of this species,

we predict its continued spread to new localities and its

establishment in native communities potentially changing

their structure and dynamics.

ACKNOWLEDGEMENTS

RA, RP and HA were funded by fellowships from the

Portuguese Foundation for Science and Technology (FCT)

through program POCI 2010, with the support of FEDER

and FSE.

Table 4. ANOVA testing for significant differences in the numberof carposporophytic and tetrasporophytic fronds (life-cycle phase)between sampling dates and rock pools.1

Source of variation df MS F

Life cycle phase (Lf) 1 8450 23.05***Date (Da) 5 10,314.5 1.85 n.s.Pool (Po) (Da) 12 5590.22 1.73 n.s.Lf 3 Da 5 1217.4 3.32*Lf 3 Po (Da) 12 366.583 0.11 n.s.Residuals 36 3223.19

Cochran’s test C 5 0.28; n.s.Transformation none

SNK test Lf 3 DaCarposporophyte 5 Tetrasporophytedate 1 (Sep.), 4 (Mar.) and 6 (Jul.)Carposporophyte . Tetrasporophytedate 2 (Nov.), 3 (Jan.) and 5 (May)

1 df, degrees of freedom; MS, mean squares; n.s., nonsignificant;*P , 0.05; ***P , 0.001.

Fig. 9. Temporal variation in the proportion of life stages (tetrasporophytes and gametophytes/carposporophytes) in the population studied.

400 Phycologia, Vol. 50 (4), 2011

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Received 27 August 2010; accepted 19 January 2011

Associate editor: Lisandro Benedetti-Cecchi

402 Phycologia, Vol. 50 (4), 2011