ORIGINAL PAPER

Illegal trawling and induced invasive algal spreadas collaborative factors in a Posidonia oceanica meadowdegradation

Sotiris Kiparissis • Elias Fakiris • George Papatheodorou •

Maria Geraga • Michael Kornaros •

Apostolos Kapareliotis • George Ferentinos

Received: 30 November 2009 / Accepted: 20 August 2010 / Published online: 18 September 2010

� Springer Science+Business Media B.V. 2010

Abstract Posidonia oceanica, a key seagrass spe-

cies of the Mediterranean Sea, shows clear signs of

regression throughout the Mediterranean and illegal

trawling is recognized as one of the main causes. We

examined the condition of a P. oceanica meadow in

Alykes Bay (Zakynthos Island, western Greece), a

typical Mediterranean littoral area where illegal

trawling is common practice, in respect to the total

area affected, and in terms of possible ecological

substitution. A side scan sonar (SSS) survey of the

seafloor provided an image of the condition of

the meadow and biological sampling evaluated the

ecological status in affected meadow areas. SSS

images revealed that trawling has a serious effect on

the meadow, with 11% of the vegetated area being

abraded, and the affected areas were also found to be

fully colonized by the invasive alga Caulerpa race-

mosa. Moreover, unusually high densities of the

polychaete Sabella pavonina were detected in the

affected areas among C. racemosa fronds. Recoloni-

zation by P. oceanica of the affected meadow areas

that have been colonized by C. racemosa seems

improbable considering the allelopathic interactions

between the species, with the alga displaying phyto-

toxic properties through caulerpenyne production and

deterioration of the sediment quality.

Keywords Posidonia oceanica � Caulerpa

racemosa var cylindracea � Mediterranean Sea �Colonization � Side Scan Sonar � Trawling

Introduction

Posidonia oceanica (L.) Delile is the dominant

seagrass species in the Mediterranean littoral zone,

forming extensive meadows down to 35–40 m depth

(Duarte 1991; Pasqualini et al. 1998). These mead-

ows have prominent ecological value for the marine

littoral ecosystems. They buffer sediment resuspen-

sion and increase sediment retention (Gacia et al.

1999; Terrados and Duarte 2000), stabilize the seabed

and prevent sandy beach erosion (Boudouresque and

Meinesz 1982), exhibit high primary production

(Peres 1977; Pergent and Pergent-Martini 1991),

S. Kiparissis (&)

Department of Aquaculture and Fisheries Technology,

Technological Educational Institute of Messolonghi,

30200 Messolonghi, Greece

e-mail: skiparis@teimes.gr

E. Fakiris � G. Papatheodorou � M. Geraga �G. Ferentinos

Laboratory of Marine Geology and Physical

Oceanography, Department of Geology, University

of Patras, 26500 Rion, Greece

M. Kornaros

Department of Chemical Engineering, University

of Patras, 26500 Patras, Greece

A. Kapareliotis

Fishery Department, Perfecture of Preveza,

Dodonis 37, 48100 Preveza, Greece

123

Biol Invasions (2011) 13:669–678

DOI 10.1007/s10530-010-9858-9

contribute to water oxygenation through photosyn-

thetic activity (Bay 1978), and constitute the basis of

the food web (Gobert et al. 2006). They offer a

variety of niches among their horizontal and vertical

rhizomes and on their leaves for a large number

of marine plant and invertebrate animal species

(Mazzella et al. 1992). They also constitute settle-

ment, nursery and adult habitat areas for a number

of Mediterranean fish species (Bell and Harmelin-

Vivien 1982; Garcia-Rubies and Macpherson 1995;

Francour 1997). P. oceanica meadows have been

identified as priority habitats for conservation under

the European Union Habitats Directive (Annex I, Dir

92/43/CEE), and protection measures have been

suggested because there are documented regression

trends of this species’ meadows throughout the

Mediterranean Sea (Peres 1984; Marba et al. 1996;

Peirano et al. 2005; Ardizzone et al. 2006).

Among the various factors primarily responsible

for this regression (such as: reduction of water clarity

due to eutrophication, alteration of sediment quality

due to human activities related to coastal develop-

ment, direct mechanical damage from different

fishing activities and anchoring (Ardizzone et al.

2006)), the impact from illegal trawling is considered

by a number of authors as being one of the most

important (e.g. Ardizzone and Pelusi 1983; Guillen

et al. 1994).

Bottom trawling inside P. oceanica meadows has a

severe impact on their condition. The otter doors work

as ploughs, eradicating the plants, while the ropes,

chain and net abrade the foliage. Recovery of the

affected P. oceanica meadows has been reported in

areas where illegal trawling has been halted. How-

ever, recovery rates for this species are very slow and

become even slower in the heavily affected areas

(Gonzalez-Correa et al. 2005). In any case, for

recovery to have an effect the sources of disturbance

would have to be eliminated and furthermore, no

substitution events would have taken place. Substitu-

tion of seagrass species by macroalgae is a worldwide

phenomenon (Montefalcone et al. 2007) and such

phenomena have also been recorded for P. oceanica.

These include cases where the invasive species

Caulerpa taxiforlia (Vahl) C. Agardh and Caulerpa

racemosa var. cylindracea (Sonder) Verlaque, Huis-

man et Boudouresque (hereafter: Caulerpa racemosa)

have colonized among other substrates and areas of

dead matte (Montefalcone et al. 2007).

Caulerpa racemosa represents one of the

most serious invasions in the Mediterranean Sea

(Ceccherelli and Piazzi 2005; Piazzi et al. 2005). This

alga was observed for the first time in the Mediterra-

nean Sea in Lybia in 1990 (Nizamuddin 1991) and

after expanding aggressively, it has been detected in

the coastal areas of twelve Mediterranean countries

(reference list in Klein and Verlaque 2008). It is

suspected to have spread throughout the Mediterra-

nean and recently its spread into the Atlantic has also

been documented (Verlaque et al. 2004). Its relationship

with the indigenous seagrass P. oceanica is presumed to

be antagonistic. While C. racemosa expansion into

degraded parts of P. oceanica meadows reaching the

fringes of the meadows, has been described as an

expected consequence of the high colonization potential

of this alga, there have been no studies or reports

evidencing the spread of this alga inside a P. oceanica

meadow as a direct impact of illegal trawling.

As part of a study conducted in the marine littoral

around Zakynthos island (Ionian Sea, western Greece),

the status of the P. oceanica meadow at Alykes Bay

was examined. Illegal trawling is common practice in

this area. Herein, we present our results concerning the

magnitude of the degradation of the meadow due to

illegal trawling, both in terms of the total area affected

and of the possible ecological substitution phenomena,

with the affected areas being fully colonized by

the invasive alga C. racemosa. We also describe

the peculiar macrofaunal situation detected in the

impacted parts of the meadow, with the polychaete

Sabella pavonina (Savigny 1820) inundating these

areas in unusually high densities.

In recent years several methods and systems have

been developed to efficiently map P. oceanica

meadows. These methods have been successfully

used to identify and quantify the anthropogenic

impacts within meadows (Pasqualini et al. 1998;

Pasqualini et al. 2000; Ardizzone et al. 2006) and

range from traditional direct methods, such as diving

for visual inspection and sampling, to indirect

methods, such as optical and hydro–acoustical meth-

ods. Among the indirect methods, the side scan sonar

(SSS) technique has been proven to be effective and

reliable in determining area distribution of seagrass

meadows (Montefalcone et al. 2006; Le Bas and

Huvenne 2009). Here, the SSS technique was used

for the mapping of the overall extent of the

P. oceanica meadow.

670 S. Kiparissis et al.

123

Methods

Study area

Alykes Bay is an open shallow bay facing the Ionian

Sea, located at the northeastern part of Zakynthos

Island (Fig. 1). The coastal environment of Alykes

Bay has been subjected to a high degree of anthro-

pogenic pressure due to marine leisure activities

(cruising boats, boating, recreational fishing and

scuba diving), professional fishing and the increasing

demand for tourist resorts.

Survey design

The mapping of P. oceanica meadow was conducted

in two phases. During the first phase, a systematic

survey of the seafloor was carried out using a side-

scan sonar. The SSS used in this survey was an

Edgetech 272 TD towfish, equipped with a transducer

emitting an acoustic signal at two frequencies (100

and 500 kHz). For the recording of the acoustic data, a

digital topside unit (Edgetech 4100P model) was used.

The acquisition software of 4100P topside recording

unit applied the geocoding to the SSS digital records,

using navigation and vessel speed data supplied from

the GPS system (model Hemisphere Crescent V100).

A 100 kHz T.V.G range signal with a slant range of

200 m per transducer on each side of the towfish was

operated. Total survey coverage spanned 6.0 km in a

southeastern—northwestern direction and about

2.0 km from the northeast to the southwest. Eight

navigation lines ran parallel to the shore 350 m apart,

to allow the SSS images (sonographs) to overlap

(Fig. 1). TritonMap (Triton Imaging Inc) software

was used to generate seafloor mosaics, which were

performed at 0.5 m resolution (Fig. 2). The SSS

mosaics were exported as GeoTIFF files for use in Arc

View GIS 9.2 (Fig. 2).

The second phase consisted of visual inspection

and biological sampling, based on the results of the

first phase, in order to produce the most accurate

information regarding seabed coverage and to vali-

date the SSS interpretation.

SSS data interpretation

The SSS sonograph provides a representation of the

seafloor in terms of backscatter. Areas of high

backscatter are associated with coarser-grained sed-

iments or hard substrate and areas of low backscatter

with relatively fine-grained sediments. In the Alykes

Bay survey, high backscatter is represented by light

tones and low backscatter by dark tones, on the

sonographs. P. oceanica meadows are distinguished

by strong backscatter which is significantly higher

than the surrounding sand-covered seafloor (Fig. 3).

The gas-filled channels (aerenchyma) within the

seagrass plants, along with the gas bubbles produced

during photosynthesis and which are found attached

to the external surfaces of the leaves, are the

dominant causes for the strong backscatter of the

seagrass meadows on the sonographs (Wilson and

Dunton 2009). Thus, the P. oceanica meadow forms

a thick layer where the gas void fraction varies with

the phase of the photosynthesis cycle. The insonifi-

cation of the seagrass meadows in Alykes Bay took

place during sunny days between 09:00 and 18:00

when photosynthesis was at its peak and thus the

backscatter was highest.

Biological sampling

Visual inspection and biological sampling was con-

ducted during August 2007 by scuba diving, in two

stations in the meadow, selected from the sonographsFig. 1 Map of Zakynthos Island, showing the study area at its

northeastern part and the side scan sonar track lines

Illegal trawling and induced invasive algal spread as collaborative factors 671

123

Fig. 2 Georeferenced side

scan sonar mosaic of the

Alykes Bay seafloor,

collected by 100 kHz

EdgeTech TD 272 side scan

sonar. Light tones represent

areas of high seabed

reflectivity while dark tonesrepresent areas of low

seabed reflectivity (see text

for details)

Fig. 3 Interpretation map

of the Alykes Bay seafloor

based on the side scan sonar

and ground-truthing data.

The two sampling stations

are also shown

672 S. Kiparissis et al.

123

(Figs. 2 and 3). Both sampling stations included

affected meadow areas. Trawling activity on the

P. oceanica meadow had created two distinct forms

of degradation: long continuous furrows about 2 m

wide, created by the otter doors in the areas where the

trawl had crossed only once (Fig. 4); wide abraded

patches of variable shape created by repetitive

crossings (Fig. 5), as evidenced by the number of

intercepting furrows. Preliminary visual survey on

the degraded parts of the meadow gave more or less

the same picture in all inspected areas, i.e., abraded or

ploughed areas with no P. oceanica shoots present,

covered by C. racemosa thalli along with high

densities of S. pavonina tubes (Fig. 6). For compar-

ative purposes, sampling for C. racemosa and

S. pavonina in Station 1 was conducted inside a

furrow and in Station 2 inside a widely abraded area.

Sampling for P. oceanica shoot densities was

conducted at both stations in neighboring intact parts

of the meadow. The depths for the two Stations

were comparable (22 m for Station 1 and 24 m for

Station 2). No abundance stratification in C. racemosa

and S. pavonina distribution was noticeable at the

sampling stations, so sampling sites within each station

were chosen randomly. Data collection included

counts of P. oceanica shoots, of C. racemosa primary

fronds and of S. pavonina live tubes in a 40 cm 9

40 cm square, which was taken as the sampling unit. In

both stations, at least 3 replicate density counts were

performed for P. oceanica, at least 4 counts for

C. racemosa and at least 5 counts for S. pavonina.

There were no live P. oceanica plants inside the

affected parts of the meadow, so shoot densities at the

two stations were compared only for their intact parts

(Student’s t-test). C. racemosa fronds were detected

among P. oceanica sheaths at Station 1 with low

frond densities, while they were found in abundance

in the affected part of the meadow. At Station 2,

C. racemosa fronds were found only in the affected

part. Due to the extremely large differences in abun-

dance between intact and affected meadow areas

Fig. 4 Posidonia oceanica meadow area affected by trawling,

showing the distinct furrow created by an otter door. The

furrow was about 2 m wide and the destroyed area was

under extensive Caulerpa racemosa colonization. (Photo by

G. Tryphonopoulos)

Fig. 5 Posidonia oceanica abraded meadow area created by

repetitive trawl crossings, with signs of older plough action of

the otter doors. All abraded meadow areas inspected were

under extensive Caulerpa racemosa colonization (Photo by

G. Tryphonopoulos)

Fig. 6 Extensive spread of the polychaete Sabella pavonina,

among Caulerpa racemosa fronds in the affected

meadow areas. Similar situations were detected in all other

degraded meadow areas that were visually inspected (Photo

by G. Tryphonopoulos)

Illegal trawling and induced invasive algal spread as collaborative factors 673

123

(see results), comparisons of the alga’s frond densi-

ties were performed only for the affected areas at the

two stations (Student’s t-test). No S. pavonina tubes

were detected inside the intact parts of the meadow

among P. oceanica shoots, so polychaete densities

were compared only for the affected parts at the two

stations (Student’s t-test).

Results

Seabed mapping

The SSS mosaic revealed four distinct acoustic facies

classified by their grey-level intensity (backscatter

intensity or reflectivity) and image texture: (1) high

reflectivity (light tones), (2) moderate reflectivity

(light grey tones), (3) narrow strips and linear features

of low reflectivity (dark grey tones) and (4) very low

reflectivity (very dark grey tones) (Fig. 2). The spatial

distribution of acoustic facies almost shows a depth

zonation pattern of the high and very low reflectivity

facies, parallel to the coastline (Fig. 2). The high

reflectivity acoustic facies represents dense, continu-

ous and almost uniform P. oceanica meadows

(Fig. 3). The seagrass meadow in the bay occupies a

surface area of about 4.2 km2 which is 43% of the

total surveyed area. The shoreward limit of the

meadow is located at a water depth of about 6 m

and the seaward limit at depths ranging from 24 to

26 m (Fig. 3). The high reflectivity patches on the

sonograph along the shoreward limit of the meadow

suggest that the nearshore limit is formed by sparse

hummocks of P. oceanica (herbier de colline)

(Fig. 2). At the northwestern part, the shorewards

and seawards limits of the meadow on the sonographs

appear continuous and sharp, suggesting that they are

regulated by natural environmental factors (hydrody-

namics, sediment balance) (Fig. 2). On the contrary,

the shorewards and seawards limits of the meadow at

the southeastern part are discontinuous and made up

of isolated shoots of P. oceanica, implying anthropo-

genic impacts (Fig. 2). The low reflectivity facies is

associated with a sandy seafloor and covers an area of

about 2.2 km2 (Figs. 2 and 3). This acoustic facies

extends from the shoreline to the shorewards limit of

the P. oceanica meadow and offshore to the seawards

limit of the meadow (Figs. 2 and 3). The moderate

reflectivity facies represents a sparse P. oceanica bed

and is in general confined to the southeastern part of

the meadow where the discontinuous depth limits

were observed (Figs. 2 and 3). The sparse P. oceanica

bed covers an area of about 2.5 km2. The narrow

strips and the linear/curvilinear features of low

reflectivity are observed within the P. oceanica

meadow (Figs. 2 and 3). These features run SE-NW

and NE-SW, in directions parallel and perpendicular

to the shoreline, having lengths ranging from 0.5 to

1.0 km (Figs. 2 and 3). Two ground-truthing stations

showed that the elongated low backscattering features

are associated with the affected parts of meadows due

to illegal trawling activity. The affected part of the

meadow covers an area of about 0.8 km2 which is up

to 11% of the total P. oceanica meadow surveyed.

Biological data

P. oceanica shoot densities in the intact parts of the

meadow at the two stations examined were found to

be significantly different (Table 1). Shoot density in

Station 1 (furrow) was lower (P \ 0.01) than that in

Station 2 (abraded area) (Fig. 7).

C. racemosa fronds were found in high densities

inside the affected meadow parts in both stations.

Frond density differences between the two stations

were highly significant (Table 1), with that in Station

1 being higher than that in Station 2. C. racemosa

thalli were also found inside the intact meadow areas

Table 1 Statistical comparisons (P values of Student’s t-test) of seagrass, alga and polychaete mean densities between the two

stations at the intact and affected meadow areas

Area Comparisons P. oceanica C. racemosa S. pavonina

Intact ST1 vs. ST2 P = 0.0021 No comparison (presence only in ST1) Not present

t = -3.113, 6 d.f.

Affected ST1 vs. ST2 Not present P \ 0.001 P = 0.066

t = 1.880, 7 d.f. t = 2.026, 12 d.f.

ST1 Station 1 (furrow), ST2 Station 2 (abraded area)

674 S. Kiparissis et al.

123

in Station 1, among P. oceanica sheaths, but in a very

low density compared with the neighboring affected

area (Fig. 7).

At Station 2, the alga had not penetrated the

meadow, as no thalli were detected inside the

sampling units, or in any other intact part of this

station that was visually inspected.

No S. pavonina tubes were detected inside the

intact parts of the meadow, while polychaete tubes

were found in high densities in the affected parts at

both stations. Density differences in the affected

areas between the two stations were not statistically

significant (Table 1), presenting a pooled mean of

184.4 tubes/m2 (±30.23 S.E., n = 14).

Discussion

According to the results obtained by the SSS images,

the P. oceanica meadow in Alykes Bay has been

seriously affected by illegal trawling, with almost

11% of the total meadow area surveyed being fully

abraded. Despite the fact that in all affected meadow

areas visually inspected, there were no live

P. oceanica shoots, we expect other affected parts

of the meadow to retain a portion of the seagrass

vegetation. The recolonization success of these

affected areas depends firstly on the effective

prevention of further illegal trawling inside the

meadow and, because C. racemosa has invaded

the area, on the outcome of the competition between

the seagrass and the alga.

Inside the furrow (Station 1), P. oceanica shoot

density was lower than that of the abraded area

(Station 2). Both these meadow areas are relatively

close and at almost the same depth. At Station 1,

C. racemosa thalli were detected among the sheaths

and rhizomes of P. oceanica, while no alga was

detected in the intact areas of Station 2. From this

study, we cannot make any safe inferences as to the

real causes of the difference in shoot densities (i.e.,

whether it is driven by local environmental condi-

tions or by competition interactions due to the alga’s

presence), since environmental monitoring was not

one of the objectives. However, coupling of the

presence of Caulerpa sp. in P. oceanica meadows

with lower seagrass shoot density has been docu-

mented (Holmer et al. 2009), and stress reaction of

P. oceanica when in contact with C. racemosa has

been demonstrated (Dumay et al. 2002). We could

assume that the lower shoot density at Station 1 is due

to a competitive interaction; however, confirmation

with further specific sampling is necessary.

Published works on C. racemosa assemblages

indicate a difficulty for the alga to penetrate dense

P. oceanica meadows, and the alga has often been

found creeping on the rhizomes at the margins of

dense meadows or inside sparse meadows (references

in Klein and Verlaque 2008). As already discussed,

C. racemosa thalli were detected among the sheaths

of P. oceanica in Station 1, even though in a low

density. Due to the relatively dense seagrass canopy

in this station, the alga’s access to light would be

limited. However, the distribution margin of 70 m

depth for this species in the Mediterranean, attests to

its high tolerance to low light conditions (Klein and

Verlaque 2008), so the presence of C. racemosa thalli

among the rhizomes and sheaths of P. oceanica in

Station 1 is justified. Absence of the alga in the intact

part of the meadow in Station 2 may be due to the

time period in which each station was available for

colonization. Furrows represent areas affected only

Fig. 7 Mean densities for P. oceanica (P.o.) (shoots/m2),

C. racemosa (C.r.) (fronds/m2) and S. pavonina (S.p.) (tubes/m2)

in the intact and the impacted parts of the meadow at the two

sampling stations. Error bars indicate ± SE

Illegal trawling and induced invasive algal spread as collaborative factors 675

123

once, and since then, they have been exposed

undisturbed to colonization. Abraded areas represent

areas affected repeatedly at different times, possibly

those that have been affected more recently. This may

also explain the lower density of C. racemosa fronds

in Station 2 (abraded area) than that in Station 1

(furrow). If the above assumption proves to be true,

then the alga may be expected to subsequently

penetrate the meadow at Station 2 as well.

No live P. oceanica shoots were detected in the

abraded areas that were fully colonized by the alga.

Whether this is the outcome of the repetitive abrasion

of the meadow or the final outcome of the compe-

tition between P. oceanica and the alga, is an issue

for further study. In any case, the point of interest is

the fate of the colonized meadow, i.e., the existence

of competitive interactions and their outcome. Com-

petitive interactions between seagrass species and this

alga have already been described; however, the full

mechanism of competition is still under investigation

and the outcome of this competitive relation has not

yet been fully elucidated. Secondary metabolites

produced by C. racemosa seem to play a major role in

its establishment and prevalence. Caulerpenyne,

being the most drastic of its secondary metabolites

(Raniello et al. 2007), exhibits phytotoxic properties

against native seagrasses, causing leaf chlorosis and

necrosis in P. oceanica (Villele and Verlaque 1995),

and reducing the photosynthetic apparatus efficiency

in Cymodocea nodosa (Raniello et al. 2007). Even

though it is not released in the environment under

normal conditions, it probably accumulates in the

substrate during cold periods, when the thalli of the

alga decompose. This process, which occurs exten-

sively in the northwestern Mediterranean during

winter (Ruitton et al. 2005) but less drastically in

the northeastern Mediterranean (Panayotidis and

Montesanto 2001), may suppress possible competi-

tors (Raniello et al. 2007). Furthermore, the deteri-

oration of the sediment quality, by increased sulfate

reduction rates and enhanced sulfide pools, has

been documented in P. oceanica meadows when

C. prolifera or C. racemosa were present (Holmer

et al. 2009). In such a case, sedimentary sulfides

accumulating in the seagrass rhizomes and roots have

been detected. This suggests a high invasion of

sulfides into the plants, a factor that has been coupled

with higher seagrass mortality (Frederiksen et al.

2007).

Considering the above, inhibition of the expansion

of P. oceanica to the affected areas already occupied

by C. racemosa may be expected. Thus, according to

current knowledge, rehabilitation of the damaged

parts of the meadow that have been colonized by the

invasive C. racemosa thalli seems improbable. This

type of degradation of the meadow, being an after-

math of illegal trawling, could develop to a more

permanent situation.

Further illegal trawling inside an already invaded

meadow would create even more favorable condi-

tions for the alga, since invaders seem to be more

successful in degraded environments (Didham et al.

2005), while further deterioration of the meadow

would also produce more space for the alga to

colonize. Moreover, because P. oceanica meadows

constitute a target for illegal trawling, such practice

inside an already colonized meadow would impose a

threat to other, remote unaffected areas, given that

C. racemosa propagates easily through vegetative

fragments (Ceccherelli and Piazzi 2001; Piazzi et al.

2003). Fragment diffusion by the trawls for Caulerpa

taxifolia, another invasive alga species, has already

been stressed in a recent work (Relini et al. 2000).

The authors stated that such fragments can be carried

several miles on a single day from the site where they

had been collected, by trawlers discarding debris and

by-catch collected on-board.

S. pavonina was found in high abundance in the

affected parts of the meadow, while no live tubes

were detected in the intact meadow areas. The

absence of S. pavonina from the intact parts of the

meadow is expected since these polychaetes are

filter-feeders, requiring open areas where the water

movement would carry suspended food items towards

them. Such open areas are created after the abrasion

of the meadow, which also provides available space

for settlement. However, it is difficult to explain the

unusually large densities in which this polychaete

was detected. A shift in macrofaunal dominance in

Moni Bay (Cyprus) after the C. racemosa spread in

the area has been detected, with polychaetes substi-

tuting gastropods in dominance (Argyrou et al. 1999).

Moreover, association of the polychate Chone spp.

with high densities of C. racemosa has also been

reported in two localities in the Canary Islands

(Verlaque et al. 2004). Environmental conditions as

modified by the presence of C. racemosa seem to

favor polychaetes, but the absolute dominance of

676 S. Kiparissis et al.

123

only one macrofaunal species, as detected in this

case, may indicate considerable ecological stress for

macrofauna.

These findings, deduced from a study in a typical

Mediterranean littoral area, offer further insight into

the impact of trawling inside P. oceanica meadows,

documenting the generation of a more severe situation

than that which has been reported so far. Since 1990,

when the invasion of C. racemosa var cylindracea

started in the Mediterranean Sea, the impact of illegal

trawling on P. oceanica meadows has acquired new

characteristics because it creates favorable conditions

for the establishment of this alga inside the meadows.

Withdrawal of P. oceanica from the affected areas

that have been colonized by C. racemosa may be

permanent, due to the alga’s high colonization

potential and its phytotoxic properties. This may

eventually render ineffective all further management

schemes for the protection of this important species.

Acknowledgments The authors wish to thank the Community

Initiative INTERREG IIIA Greece—Italy 2000–2006 for the

financial support for this work under Grant No I3101024

(Acronym: GoW). We would also like to thank Dr G.

Tryphonopoulos for aiding in the biological data collection

and photographs, A. Koutsodendris for his assistance during the

SSS data acquisition, Professor S. Sfendourakis for his valuable

comments on the manuscript and Mrs A. Mullholland for

comments on the language.

References

Ardizzone G, Pelusi P (1983) Regression of a Tyrrhenian

Posidonia oceanica prairie exposed to nearshore trawling.

Rapp Comm Int Mer Medit 28:3

Ardizzone G, Belluscio A, Maiorano L (2006) Long-term

change in the structure of a Posidonia oceanica landscape

and its reference for a monitoring plan. Mar Ecol

27:299–309. doi:10.1111/j.1439-0485.2006.00128.x

Argyrou M, Demetropoulos A, Hadjichristophorou M (1999)

Expansion of the macroalga Caulerpa racemosa and

changes in softbottom macrofaunal assemblages in Moni

Bay, Cyprus. Oceanol Acta 22:517–528

Bay D (1978) Etude in situ de la production primaire d’un herbier

de Posidonies (Posidonia oceanica (L.) Delile) de la baie de

Calvi-Corse. Dissertation, University of Liege, Belgium

Bell JD, Harmelin-Vivien M (1982) Fish fauna of French

mediterranean Posidonia oceanica seagrass meadows. 1.

Community structure. Tethys 10:337–347

Ceccherelli G, Piazzi L (2001) Dispersal of Caulerpa race-mosa fragments in the Mediterranean: lack of detachment

time effect on establishment. Bot Mar 44:209–213. doi:

10.1515/BOT.2001.027

Ceccherelli G, Piazzi L (2005) Exploring the success of manual

eradication of Caulerpa racemosa var. cylindracea (Ca-

ulerpales, Chlorophyta): the effect of habitat. Cryptogam

Algol 26:319–328

Didham RK, Tylianakis JM, Hutchinson MA, Ewers RM,

Gemmell NJ (2005) Are invasive species the drivers of

ecological change? Trends Evol Ecol 20:470–474. doi:

10.1016/j.tree.2005.07.006

Duarte CM (1991) Allometric scaling of seagrass form and

productivity. Mar Ecol Prog Ser 77:289–300. doi:0171-

8630/91/0077/0289/$03.00

Dumay O, Fernandez C, Pergent G (2002) Primary production

and vegetative cycle in Posidonia oceanica when in

competition with the green algae Caulerpa taxifolia and

Caulerpa racemosa. J Mar Biol Assoc UK 82:379–387

Francour P (1997) Fish assemblages of Posidonia oceanicabeds at port-cros (France, NW Mediterranean): assess-

ment of composition and long-term fluctuations by visual

census. P.S.Z.N. Mar Ecol 18:157–173. doi:10.1111/

j.1439-0485.1997.tb00434.x

Frederiksen MS, Holmer M, Dıaz-Almela E, Nuria M, Duarte C

(2007) Sulfide invasion in the seagrass Posidonia oceanicaat Mediterranean fish farms: assessment using stable sulfur

isotops. Mar Ecol Prog Ser 345:93–104. doi:10.1016/

j.marpolbul.2008.05.020

Gacia E, Granata TC, Duarte CM (1999) An approach to

measurement of particle flux and sediment retention

within seagrass (Posidonia oceanica) meadows. Aquat

Bot 65:255–268. doi:10.1016/S0304-3770(99)00044-3

Garcia-Rubies A, Macpherson E (1995) Substrate use and

temporal pattern of recruitment in juvenile fishes of the

Mediterranean littoral. Mar Biol 124:35–42

Gobert S, Cambridge ML, Velimirov B, Pergent G, Lepoint G,

Bouquegneau JM, Dauby M, Pergent-Martini P, Walker

DI (2006) Biology of Posidonia. In: Larkum AWD, Orth

RJ, Duarte CM (eds) Seagrasses: biology, ecology and

conservation. Springer Verlag, Berlin, pp 387–408

Gonzalez-Correa JM, Bayle JT, Sanxhez-Lizaso JL, Valle C,

Sanchez-Jerez P, Ruiz J (2005) Recovery of deep Posi-donia oceanica meadows degraded by trawling. J Exp

Mar Biol Ecol 320:65–76. doi:10.1016/j.jembe.2004.

12.032

Guillen JE, Ramos AA, Martınez L, Sanchez-Lizaso JL (1994)

Antitrawling reefs and the protection of Posidonia ocea-nica (L.) Delile meadows in the western Mediterranean

Sea: demand and aims. Bull Mar Sci 55:645–650

Holmer M, Marba N, Lamote M, Duarte CM (2009) Deterio-

ration of sediment quality in seagrass meadows (Posidoniaoceanica) invaded by macroalgae (Caulerpa sp.). Estuar

Coast 32:456–466. doi:10.1007/s12237-009-9133-4

Klein J, Verlaque M (2008) The Caulerpa racemosa invasion:

a critical review. Mar Pollut Bull 56:205–225. doi:

10.1016/j.marpolbul.2007.09.043

Le Bas TP, Huvenne VAI (2009) Acquisition and processing of

backscatter data for habitat mapping–comparison of mul-

tibeam and sidescan systems. Appl Acoust 70:1248–1257.

doi:10.1016/j.apacoust.2008.07.010

Marba N, Duarte CM, Cebrian J, Gallegos ME, Olesesn B,

Sand-Jensen K (1996) Growth and population dynamics

of Posidonia oceanica on the Spanish Mediterranean

Illegal trawling and induced invasive algal spread as collaborative factors 677

123

coast: elucidating seagrass decline. Mar Ecol Prog Ser

137:203–213

Mazzella L, Buia M, Gambi MC, Lorenti M, Russo GF,

Scipione MB, Zupo V (1992) Plant-animal trophic rela-

tionships in the Posidonia oceanica ecosystem of the

Mediterranean Sea: a revue. In: John DM, Hawkins SJ,

Price JH (eds) Plant-animal interactions in the marine

benthos. Clarendon Press, Oxford, pp 165–187

Montefalcone M, Albertelli G, Bianchi CN, Mariani M, Morri

C (2006) A new synthetic index and a protocol for mon-

itoring the status of Posidonia oceanica meadows: a case

study at Sanremo (Ligurian Sea, NW Mediterranean).

Aquat Conserv Mar Freshw Ecosyst 16:29–42. doi:

10.1002/aqc.688

Montefalcone M, Morri C, Peirano A, Albertelli G, Bianchi CN

(2007) Substitution and phase shift within the Posidoniaoceanica seagrass meadows of NW Mediterranean Sea.

Estuar Coast Shelf Sci 75:63–71. doi:10.1016/j.ecss.

2007.03.034

Nizamuddin M (1991) The green marine algae of Libya. Elga

publisher, Bern

Panayotidis P, Montesanto B (2001) Occurrence and phyto-

sociology of Caulerpa racemosa in Saronikos Gulf

(Aegean Sea, Greece). In: Gravez V, Ruitton S, Bou-

douresque CF, Le Direac’h L, Meinesz A, Scabbia G,

Verlaque M (eds) Fourth international workshop on

Caulerpa taxifolia. GIS Posidonie Publ, Marseilles,

France, pp 334–337

Pasqualini V, Pergent-Martini C, Clabaut P, Pergent G (1998)

Mapping of Posidonia oceanica using aerial photographs

and side-scan sonar: application of the island of Corsica

(France). Estuar Coast Shelf Sci 47:359–367. doi:10.1006/

ecss.1998.0361

Pasqualini V, Clabaut P, Pergent G, Benyoussef L, Pergent-

Martini C (2000) Contribution of side scan sonar to the

management of Mediterranean littoral ecosystems. Int J

Remote Sens 21:367–378. doi:10.1080/014311600210885

Peirano A, Damasso V, Montefalcone M, Morri C, Bianchi CN

(2005) Effects of climate. invasive species and anthro-

pogenic impacts on the growth of the seagrass Posidonia

oceanica (L.) Delile in Liguria (NW Mediterranean Sea).

Mar Pollut Bull 50:817–822. doi:10.1016/j.marpolbul.

2005.02.011

Peres J (1977) Utilite et importance de l’herbier de Posidonies

en Mediterranee. Bull Off Nat Peches Tunissie 1:3–8

Peres J (1984) La regression des herbiers a Posidonia ocea-nica. In: Boudouresque CF, Jeudy de Crissac A, Olivier J

(eds) International workshop on Posidonia oceanica beds.

GIS Posidonie Publ, Marseille, France, pp 445–454

Pergent G, Pergent-Martini C (1991) Leaf renewal cycle and

primary production of Posidonia oceanica in the bay of

Lacco Ameno (Ischia, Italy) using lepidochronological

analysis. Aquat Bot 42:49–66

Piazzi L, Ceccherelli G, Balata D, Cinelli F (2003) Early

patterns of Caulerpa racemosa recovery in the Mediter-

ranean Sea: the influence of algal turfs. J Mar Biol Assoc

UK 83:27–29. doi:10.1017/S0025315403006751h

Piazzi L, Balata D, Ceccherelli G, Cinelli F (2005) Interactive

effect of sedimentation and Caulerpa racemosa var.cylindracea invasion on macroalgal assemblages in the

Mediterranean Sea. Estuar Coast Shelf Sci 64:467–474.

doi:10.1016/j.ecss.2005.03.010

Raniello R, Mollo E, Lorenti M, Gavagnin M, Buia MC (2007)

Phytotoxic activity of caulerpenyne from the Mediterra-

nean invasive variety of Caulerpa racemosa: a potential

allelochemical. Biol Invasions 9:361–368. doi:10.1007/s10530-006-9044-2

Relini G, Relini M, Torchia G (2000) The role of fishing gear

in the spreading of allochthonous species: the case of

Caulerpa taxifolia in the Ligurian Sea. ICES J Mar Sci

57:1421–1427. doi:10.1006/jmsc.2000.0913

Ruitton S, Verlaque M, Boudouresque CF (2005) Seasonal

changes of the introduced Caulerpa racemosa var. cy-lindracea (Caulerpales, Chlorophyta) at the northwest

limit of its Mediterranean range. Aquat Bot 82:55–70. doi:

10.1016/j.aquabot.2005.02.008

Terrados J, Duarte CM (2000) Experimental evidence of

reduced particles resuspension within a seagrass (Posi-donia oceanica) meadow. J Exp Mar Biol Ecol 243:

45–53. doi:10.1016/S0022-0981(99)00110-0

Verlaque M, Afonso-Carrillo J, Candelaria GRM (2004) Blitz-

krieg in a marine invasion: Caulerpa racemosa var.

cylindracea (Bryopsidales, Chlorophyta) reaches the Can-

ary Islands (north-east Atlantic). Biol Invasions 6:269–281.

doi:10.1023/B:BINV.0000034589.18347.d3

Villele De X, Verlaque M (1995) Changes and degradation in a

Posidonia oceanica bed invaded by the introduced tropi-

cal alga Caulerpa taxifolia in the north western Mediter-

ranean. Bot Mar 38:79–87

Wilson PS, Dunton KH (2009) Laboratory investigation of the

acoustic response of seagrass tissue in the frequency band

0.5–2.5 kHz. J AcoustSocAm 125:1951–1959. doi:10.1121/

1.3086272

678 S. Kiparissis et al.

123