Content uploaded by Arnaud Abadie
Author content
All content in this area was uploaded by Arnaud Abadie on Oct 19, 2017
Content may be subject to copyright.
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
From mechanical to chemical impact of anchoring in seagrasses: The
premises of anthropogenic patch generation in
Posidonia oceanica
meadows
Arnaud Abadie a,d,c ,Pierre Lejeune a, Gérard Pergentc, Sylvie Gobert
a
Station de Recherches Sous-marines et Oceanographiques (STARESO), Pointe Revellata, BP 33,20260
Calvi, France b Laboratory of Oceanology. MARE Centre, University of Liege. B6C, 4000 LIEGE, Sart
Tilman, Belgium
c
EqEL-FRES 3041, UMR CNRS SPE 6134, University of Corsica, 20250 Corte, France
ABSTRACT
Intensive anchoring of leisure boats in seagrass meadows leads to mechanical damages. This
anthropogenic impact creates bare mat patches that are not easily recolonized by the plant. Several
tools are used to study human impacts on the structure of seagrass meadows but they are not able to
assess the indirect and long term implication of mechanical destruction. We chose to investigate the
possible changes in the substrate chemistry given contrasted boat impacts. Our observations show
that hydrogen sulfide concentrations remain high at 15 and 20 m depth (42.6 µM and 18.8 µM) several
months after the highest period of anchoring during the summer. Moreover, our multidisciplinary
study reveals that anchoring impacts of large boats at 15 and 20 m depth can potentially change the
seascape structure. By taking into account both structural and chemical assessments, different
managing strategies must be applied for coastal areas under anthropogenic pressures.
Keywords:
Anchoring; Conservation; Seagrass; Seascape; Patch
1. Introduction
Over the last decades, marine ecosystems all around the world have been facing impacts of human
activities at various extents (Halpern et al. 2008; Jorda et al. 2012). This statement is particularly
observed in the Mediterranean Sea at the level of the coastal habitat formed by seagrass meadows
(Grech et al. 2012; Giakoumi et al. 2013). Seagrasses play a major ecological and economical role at the
level of the global ocean, covering an area reaching up to 500,000 km2 (Costanza et al. 1997; Short et
al. 2007; Cullen-Unsworth and Unsworth 2013). Thus, they constitute a nursery (Beck et al. 2001), a
large carbon sink (Fourqurean et al. 2012), as well as a protection against coastal erosion by
attenuating waves and currents (Ondiviela et al. 2014). Among Mediterranean seagrasses,
Posidonia
oceanica
(L.) Delile is the most studied due to its major ecological and economical role (Ruiz et al.
2009; Vassallo et al. 2013). The meadows it forms are observed from the surface to 40 m depth and are
subject to the impact of human activities like coastal development, eutrophication, trawling, fish farms
and anchoring (Boudouresque et al. 2009; Giakoumi et al. 2015b).
Along the French Mediterranean coasts, the main substrate affected by boat anchoring appear to be
Posidonia oceanica
(Holon et al. 2015). Anchoring inside
P
.
oceanica
meadows seems to have various
degrees of impact according to its density, frequency, the type of anchor and the depth as well as the
size of boats (Boudouresque et al. 2012). Thus, repeated anchoring of cruise ships, at depths greater
than 15 m, causes large-scale degradations of the meadows (Ganteaume et al. 2005b; Abadie et al.
2015). In the same way small units, less than 10 m long, can have an important impact at a local scale
(Francour et al. 1999; Milazzo et al. 2004; Ceccherelli et al. 2007).
At the present day, studies mainly targeted the degradation of small boats at shallow depths i.e. less
than 10 m. Few works treat the effects of larger pleasure ships anchoring which can measure more
than 80 m long and have an important impact in confined areas (Abadie 2012). In order to assess their
impact, several parameters are classically measured: the meadow density, the mat structure and the
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
bottom cover (Boudouresque et al. 1995; Francour et al. 1999; Pergent-Martini et al. 2005). However,
some of these metrics seem not relevant enough to assess the damages observed on P.
oceanica
meadows. More specifically, classical indicators can indicate a good state of conservation of the
meadow with no anthropogenic impact when tracks of bare mat (Fig. 1a) are clearly observed (Milazzo
et al. 2004; Ganteaume et al. 2005a).
Intensive anchoring can lead to modifications of substrate qualities, passing from meadows to large
bare mat areas in which anchoring tracks are visible (Fig. 1b). This phenomenon also induces a change
in sediments nature going from carbonate sediments possibly oxygenized by the living plant to fine
particles filling crevices inside decomposing organic tissues forming an anoxic bare mat (Mateo and
Romero 1997). Such evolution of the substrate qualities can lead to the hydrogen sulfide (H2S)
intrusion in healthy meadows of the area, limiting the plant development (Holmer et al. 2003; Marbà et
al. 2006). Thus, it has been observed that in carbonate sediments H2S concentrations higher than 10
µM can cause a limitation of P.
oceanica
growth (Calleja et al. 2007).
This study aims to trigger a new way to approach the study of the anchoring impact on seagrass
meadows by (1) testing the relevance of the classical structural tools (e.g. meadow density and cover,
mat compactness); (2) exploring the relevance of chemical properties of the sediment as a new tool;
and by extension; (3) assessing the impact of large leisure ships in a confined area; and lastly, (4)
investigating the possible consequences for management and conservation of the areas concerned
correlated with anchoring pressure.
Fig. 1. a) Anchoring track inside a
P. oceanica
meadow at 30 m depth in CalviBay (Corsica, France); b)
Bare mat
of Posidonia oceanica
generated by intensive anchoring at 18 m depth in Calvi Bay (Corsica,
France) with furrows dug by large ships (photos: Arnaud Abadie).
2. Material and methods
This study was conducted in Alga Bay (8°43'52" E; 42°34'20" N), an area of 1 km2 of intensive anchoring
in Calvi Bay (Corsica, France), colonized by a
P. oceanica
meadow covering 0.78 km2 (Fig. 2). This site
encompasses a particular structure called "return river", a large sand patch where no seagrass meadow
can grow, possibly due to strong bottom currents deriving from the surface ones reflected by the coast
as described by Boudouresque and Meinesz (1982).
Six stations on two different sites in Calvi Bay were studied at three different depths, i.e. 10 m, 15 m
and 20 m. Three stations were chosen as control in a continuous meadow with no traces of impact
from human activities near the research facility of STARESO (C10, C15 and C20). Three stations were
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
sampled at Alga Bay in areas of intensive anchoring (A10, A15 and A20) where it can generate
anthropogenic patches.
Fig. 2. Map of the study site. Green polygons in Calvi represent the mapping
of Posidonia oceamica
meadows realized with data of 2010 (Abadie 2012).
2.1. Anchoring pressure assessment
A boat counting in Alga Bay was daily performed in the afternoon from May to October 2014 (the
touristic period in Corsica) where anchoring frequency is the higher. Ships sizes were classified in three
categories according to their length: <10 m; 10-20 m; and >20 m. In parallel, the substrate of
anchoring (meadow, rock or sand) was assessed. Moreover, the spatial distribution of boats anchored
in the area was investigated by using AIS positioning system of leisure boats (www.marinetraffic.com)
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
from 2012 to 2014 as well as direct catches obtained between 2012 and 2014. These observations were
inserted in the G1S software ArcGis® 10 coupled with a map of P.
oceanica
meadows in the area from
previous studies (Michel et al. 2012; Jousseaume et al. 2013; Richir et al. 2015).
2.2. Meadow structure
The impact of anchoring on the
P. oceanica
meadows was assessed using six metrics commonly used
in the study of its impact on seagrass meadows, i.e. the density, the proportion of
orthotropic/plagiotropic rhizomes, the mat compactness, and the rhizomes baring. Ten replicates of
the meadow density were randomly counted using quadrats of 25 cm x 40 cm and classified according
to the grid of UNEP-MAP-RAC/ SPA (2011). Assessment of the proportion of orthotropic/plagiotropic
rhizomes was performed during density measures and interpreted thanks to the classes made by
Charbonnel et al. (2000) (Table 1). Mat compactness was investigated given the method and
classification of Francour et al. (1999) using a 1 m long rod and a 5 kg weight, repeating ten times the
measure for each station (Table 1). Twenty replicates per station of the rhizomes baring, i.e. the
distance between rhizome and substrate, were measured and classified according the protocol of
Boudouresque et al. (1980). Meadow cover was measured using a 30 cm x 30 cm quadrat hold at arm-
length 3 m above the meadow (Gravez et al. 1995). Thirty replicates were performed for this measure
and results were interpreted given the scale of Charbonnel et al. (2000) (Table 1). This measure was
standardized by keeping the same observer for all measures and placing a depth gauge on the
quadrat in order to avoid a distance variation from the vegetation. Finally, 20 longest standing leaves
per station (corresponding to the canopy height) were measured in September after the touristic
period).
2.3. Conservation Index (CI)
The Conservation Index (CI) was used as a reflection of damages in
P. oceanica
meadows visually
observed by scuba diving. Triplicate transects were made to calculate the CI for each station according
to the process of Moreno et al. (2001) :
CI = L/(L + D)
where L (%) corresponds to the proportion of living
P. oceanica
and D (%) the percentage of bare mat.
Four intervals were calculated to assess the meadow's state of conservation on each station:
1. CI<(xmean-1/2s)
2. CI from (xmean-1/2s) to xmean
3. CI from xmean to (xmean+1/2s)
4. CI>(xmean+1/2s)
where mean (xmean) and standard deviation (s) were calculated from all Cl values of the study.
2.4. Sediment chemistry and nutrients
Sediment chemistry was studied by sampling pore water in the control (C) and anchoring (Am)
meadow, as well as in anchoring bare mat patches' sediments (Ap) given the method of Gobert et al.
(2006). Collection was performed in September after the warmest period of the year and in November
when seawater temperature starts to decrease.
Thus, the concentration of several essential components was studied in the substrate: dissolved
dioxygen (O2), free hydrogen sulfides (H2S) and nutrients.
The pore water sampling for O2 measurements was made within the oxygenic layer at a maximum
depth of 1 cm in the sediments. O2 concentration was obtained using a iodine titration with thiosulfate
according to the method of Winkler (1888) with an automatized system for small sampling volumes
(Carpenter 1965; Strickland and Parsons 1972) adapted by R. Biondo, (Laboratory of Oceanology-
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
University of Liège).
The sample collection for H2S and nutrient analysis was performed in triplicates inside the layer
encompassing the plant living parts at 10 cm depth in the substrate. H2S concentration was measured
with a silver/ sulfide ISM-146 FTH 25-XS electrode, coupled with a Sulfide
Anti-
Oxydant Buffer (SAOB)
solution given the protocol of Brooks (2001). For detailed protocols of the measure of O2 and H2S, see
Appendix S1 and S2 in supplementary material. Ammonium (NH4+) and Nitrite (NO2-)/ Nitrate (NO3-)
concentrations were measured by using a SKALAR auto-analyzer following the method of Aminot and
Kérouel (2007) adapted for oligotrophic samples (Laboratory of Oceanology-University of Liège).
Table 1: Meadow structure parameter interpretation according to their value.
Parameter
Unit
Range
Interpretation
Classification reference
Meadow density
Shoots.m-2
Depends of depth
High
Good
Normal
Moderate
Bad
UNEP-MAP-RAC/SPA 2011
Proportion of
orthotrophic/plagiotropic
rhizomes
%
<30%
30 to 70%
>70%
Stable meadow
Slight trend to progress
Net trend to progress
Charbonnel et al. 2000
Mat compactness
cm
<50cm
50 to 100 cm
>100 cm
Strong compactness
Medium compactness
Weak compactness
Francour et al. 1999
Rhizomes baring
cm
<5cm
5 to 15 cm
>15cm
Low baring
Medium baring
High baring
Boudouresque et al. 1980
Meadow cover
%
>80%
60-80%
40-60%
20-40%
<20%
Very high covering
High covering
Medium covering
Low covering
Very low covering
Charbonnel et al. 2000
2.5. Statistical analyses
Statistical analyses were performed under the R 3.0.2 software using the FactoMineR package.
Normality of structural parameters values was checked using a Shapiro-Wilk test. Stations were then
statically tested two by two (control vs anchoring) for each depth (10 m, 15 m and 20 m) with an
unpaired t-test (after checking their homoscedasticity with a Fisher test) for Gaussian data, and with a
Mann Whitney test for non-parametric ones.
T
-tests were followed by a Tukey post-hoc test and Mann
Whitney tests by a Dunns test.
Relations between the structural (i.e. meadow density, mat compactness, rhizomes baring, meadow
cover, plagiotropic/orthotropic rhizomes proportion, Conservation Index and canopy height) and
chemical (i.e. O2, H2S and NH4+ concentrations) parameters were investigated with a Pearson matrix of
correlation.
Finally, a cluster analysis was performed using the Ward method of aggregation and Euclidean
distances between individuals for testing dissimilarity. Clusters were thus defined by minimizing the
loss of inertia (i.e. the Euclidean distance) between several individuals (i.e. stations) when grouping
them. Prior to the analyses, data were standardized to take into account the difference of units. First,
structural parameters alone were considered. Then only chemical features were used. Finally, both
structural and chemical parameters were computed in order to study the impact of chemical
parameters on the evaluation of the meadows' state of conservation.
3. Results
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
3.1. Ships: spatial distribution and frequenting
The spatial ship distribution in Alga Bay follows a bathymetrical zo-nation according to data from 2012
to 2014 (Fig. 3). Small boats (length < 10 m) appear to anchor at shallow depths (< 5 m, Fig. 3). The
majority of ships measuring between 10 and 20 m prefers to anchor outside the meadow in the main
part of the return river at depths shallower than 15 m, when bigger ships choose to lay their anchors in
the meadow from 10 to 30 m depth (Fig. 3).
Anchoring substrates vary widely according to ship sizes in Alga Bay (Fig. 3). Sand appears to be the
preferred anchoring substrate for small boats (53%, Fig. 3) while those of medium and large size chose
P. oceanica
meadows (respectively 55% and 84%, Fig. 3). In general, ships anchor equally in sand (45%)
and meadow (47%), few anchoring on rock (8%, Fig. 3).
A total of 1768 ships anchoring in Alga Bay were observed from May to October 2014, encompassing
43% (754 ships) of small boats (length < 10 m), 53% (935 ships) of medium size (length 10-20 m) and
7% (79 ships) of large size (length > 20 m) (Fig. 4). Period of most intense anchoring occurs from mid -
July to mid-August, reaching a frequenting peak of 74 ships the 7th of August (Fig. 4).
3.2. Meadow structure and conservation
Meadow densities are classified as "normal" according to their depths for two control (C) stations (C10
and C20) and all anchoring (A) stations A10, A15 and A20 (Fig. 5a). The control station at 15 m depth
appears as "good" (437 ± 112 shoots.m-1). Mean values of meadow density obtained at 15 m depth are
significantly different (t-test:
t
= 892;
p
= 0.0097; df = 18). The same statement is made concerning the
proportion of orthotropic/plagiotropic rhizomes which correspond to a stable meadow for all stations
(Fig. 5e) except for the station A20 which is considered to have a "slight trend to progress" (70/30 ±
25%). Mat compactness is characterized as "strong" for all stations sampled (Fig. 5b) with the
exception of A20 with a "medium" mat compactness revealed by a relatively high penetration length of
the rode (51 ± 9 cm). A significant difference (
t
-test:
t
= 6.172;
p
< 0.0001; df = 18) of the compactness
was observed at 20 m between the control station and the anchoring one. Rhizomes baring is
"medium" for all stations except for C10 (3.6 ± 1.9 cm) and A20 (2.0 ± 1.1 cm) where it is "weak" (Fig.
5c), these differences at 10 m (
t
-test:
t =
4.493;
p =
0.0001; df = 28) and 20 m (Mann Whitney test:
p =
0.0002; U = 24) being confirmed by the statistical analysis. Meadow cover varies from "very high" (C10,
C15, and A10) to "high" (C20, A15 and A20) (Fig. 5d), thus highlighting a difference of the mean
meadow cover between the control station and the anchoring one at 15 m depth (Mann Whitney test:
p <
0.0001; U = 182.5). At last, canopy height shows no significant differences between control and
anchoring stations, its value decreasing from June to September at all depths (Fig. 5f).
The state of conservation of each control station, expressed by the Conservation index (CI), is the
higher for C10 and C15 (1 ± 0.00 for each station), and decreases (0.98 ± 0.03) for C20 (Table 2). At
Alga Bay, the anchoring site, the station at 10 m depth (A10) appears to have a state of conservation
(CI = 0.97 ± 0.03) similar to C20 while the deeper station stations (A15 and A20) have a lowest one
(with a Cl of respectively 0.85 ± 0.11 and 0.79 ± 0.15; Table 2).
Table 2 : Interpretation scale of the Conservation Index (CI) and its mean value (± SE). C: control; A:
anchoring. 10, 15 and 20: depth.
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
Fig. 3. Ship positioning using AIS and direct catches from 2012 to 2014 at Alga Bay coupled with a
map of marine habitats and proportion of anchoring on the three different substrates in 2014 for ships
with a length lower than 10 m; between 10 and 20 m, upper than 20 m and for all classes.
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
Fig. 4. Daily boat counting and size classes from June to September 2014 in Alga Bay.
3.3. Patch and meadow chemistry
In September, lowest concentrations of O2 were found inside the patch at -10 m (Ap10: 102.7 µM)
while a decrease with the depth in control meadows is observed (Table 3). The same pattern is
observed in November with concentrations similar in both control (C) and anchoring (Am) meadows.
Low concentrations in O2 are related to high concentration in H2S inside the patches at the three
depths in September (20.5 µM at -10 m; 9.9 µM at 15 m; 12.8 µM at 20 m). High sulfide concentrations
are also found in control meadows in September, except at 15 m (Table 3). In November, H2S
concentrations are relatively low at -10 m for all stations when they remain high at 15 and 20 m
(except for C15).
NO2- and NO3- show very low concentrations in both September and November. NH4+ shows in
September an increase of its concentration along with the depth (Table 3), as well as higher values
inside anchoring patches (except for Ap15). The same pattern is observed in November with the
exception that lower values are found in anchoring patches at 10 m instead of 15 m (Table 3).
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
Fig. 5. Mean value (± SE) at 10,15 and 20 m depth of a) meadow density (green: good; yellow: normal)
; b) penetration length (green: high compactness; yellow: medium compactness); c) rhizomes baring
(green: weak; yellow: medium); d) meadow cover (blue: very high covering; green: high covering); e)
orthotropic/plagiotropic rhizomes proportion, colored bar: orthotropic, white bar: plagiotropic (green:
stable meadow; yellow: slight trend to progress); f) mean canopy height" above a pair of bars indicates
a significant difference between the two mean values. C = control; A = anchoring; j = June; s =
September.
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
Table 3 : Concentration of dissolved oxygen (O2) within the first centimeter of substrate and mean
concentration of free hydrogen sulfides (H2S), nitrite (NO2-), nitrate (NO3-) and ammonium (NH4+) in
the first ten centimeters of substrates (± SE) in September (Sep.) and November (Nov.) at control (C),
anchoring meadow (Am) and anchoring patch (Ap) stations.
O2(µM)
H2S (µM)
NO2- (µM)
NO3- (µM)
NH4+
(µM)
Station
Sep.
Nov.
Sep.
Nov.
Sep.
Nov.
Sep.
Nov.
Sep.
Nov.
C10
206.0
226.8
39.1 (±37.7)
4.0 (±1.1)
0.06 (±0.00)
0.20 (±0.12)
0.22 (±0.09)
1.92 (±1.54)
4.68 (±2.44)
4.40 (±1.56)
Am10
232.7
213.4
12.0 (±12.4)
4.2 (±0.8)
0.08 (±0.03)
0.06 (±0.00)
0.22 (±0.09)
0.30 (±0.21)
4.74 (±1.78)
4.44 (±0.87)
Ap10
102.7
143.6
20.5 (±30.2)
9.3 (±4.7)
0.06 (±0.00)
0.06 (±0.00)
0.14 (±0.03)
0.24 (±0.00)
10.18 (±8.13)
2.76 (±0.22)
C15
195.1
199.6
0.4 (±0.5)
8.0 (±5.3)
0.06 (±0.00)
0.08 (±0.03)
0.42 (±0.31)
0.38 (±0.18)
10.34 (±6.21)
6.32 (±3.81)
Am15
145.2
189.3
8.1 (±8.4)
33.4 (±44.7)
0.12 (±0.00)
0.08 (±0.03)
0.76 (±0.70)
0.42 (±0.33)
10.76 (±5.38)
12.38 (±8.65)
Ap15
116.9
122.0
9.9 (±7.2)
42.6 (±56.2)
0.08 (±0.03)
0.06 (±0.00)
0.16 (±0.03)
0.22 (±0.12)
6.70 (±3.47)
16.82 (±7.69)
C20
191.8
210.8
16.5 (±21.9)
20.9 (±19.4)
0.08 (±0.03)
0.08 (±0.03)
0.30 (±0.16)
0.34 (±0.19)
14.38 (±7.99)
7.44 (±3.31)
Am20
177.7
211.5
0.9 (±0.8)
13.2 (±16.1)
0.08 (±0.03)
0.08 (±0.03)
0.40 (±0.34)
0.26 (±0.09)
13.82 (±9.51)
7.70 (±5.77)
Ap20
155.5
183.6
12.8 (±21.0)
18.8 (±8.3)
0.06 (±0.00)
0.10 (±0.07)
0.16 (±0.07)
0.50 (±0.45)
20.74 (±26.40)
13.14 (±15.02)
Table 4 : Pearson's matrix of correlation comparing both structural and chemical parameters of the
control and anchoring meadow at a depth of 10,15 and 20 m. Density: meadow density; Compact: mat
compactness; Rhiz. Bar.: rhizome baring; Cover: meadow cover; Ortho. prop.: Orthotropic rhizomes
proportion; CI: conservation index; ch: canopy height; o2: oxygen; h2 s: hydrogen sulfide; nh4:
ammonium; j: June; s: September; n: November.
Variables
Density
Compact
Rhiz. Bar.
Cover
Ortho.
prop.
CI
ch_j
ch_s
o2_s
o2_n
h2s_s
h2s_n
nh4_s
nh4_n
Density
1
-0.556
0.463
0.876
0.703
0.740
0.720
0.696
0.660
0.282
0.410
-0.635
-0.900
-0.618
Compact.
1
-0.478
-0.369
-0.669
-0.787
-0.570
-0.462
-0.259
-0.146
-0.667
-0.004
0.452
0.180
Rhiz. Bar.
1
0.159
0.367
0.354
0.204
-0.096
0.360
-0.251
-0.063
0.052
-0.405
-0.041
Cover
1
0.681
0.652
0.896
0.881
0.812
0.689
0.588
-0.872
-0.889
-0.864
Ortho. prop.
1
0.972
0.807
0.492
0.794
0.464
0.430
-0.626
-0.470
-0.760
CI
1
0.763
0.530
0.658
0.364
0.496
-0.509
-0.492
-0.639
ch_j
1
0.848
0.852
0.826
0.767
-0.761
-0.744
-0.875
ch_s
1
0.533
0.752
0.857
-0.648
-0.814
-0.668
o2_s
1
0.687
0.329
-0.871
-0.612
-0.941
o2_n
1
0.710
-0.731
-0.438
-0.818
h2s_s
1
-0.289
-0.569
-0.427
h2s_n
1
0.594
0.961
nh4_s
1
0.574
nh4_n
1
3.4. Computation of structural and chemical parameters
Among the structural parameters, rhizome baring (Rhiz. Bar.) appears to have weak correlation with all
the other one (Table 4). Mat compactness (Compact.) appears to be less correlated with meadow cover
(Cover) and the canopy height in June (ch_j), this last parameter having also few links with the
proportion of orthotropic/plagiotropic rhizomes (Ortho. Prop.; Table 4). Between chemical parameters,
H2S concentrations in November (h2s_n) show a strong correlation with O2 (o2_n) and NH4+ (nh4_n)
ones at the same period (Table 4). This link is not found in September where only H2S and NH4+
concentrations are correlated. Through the two different periods, oxygen in September (o2_s) is
strongly correlated with the hydrogen sulfide in November (h2s_n) and ammonium (nh4_n). Looking at
both structural and chemical parameters, all chemical parameters appear correlated with meadow
cover (Cover) and canopy height (ch_j and ch_s) and to a lesser extent with meadow density (Density;
Table 4). In contrary, both mat compactness (Compact.) and rhizome baring (Rhiz. Bar.) are not linked.
These observations are more contrasted concerning the proportion of orthotropic/plagiotropic
rhizomes (Ortho. Prop.) and the Conservation Index (CI) where correlations are only found in
November for H2S and NH4.
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
The cluster analysis computing the structural parameters alone shows three classes linking anchoring
stations at 15 and 20 depths (A15 and A20), when the two control meadows corresponding (C15 and
C20) are grouped with the anchoring station at 10 m (A10), leaving the control one (C10) within a
single class (Fig. 6a). When using only chemical features the cluster result changes, aggregating the
stations A10 and C10 together and grouping C15, C20 and A20, leaving A15 alone (Fig. 6b). Adding the
chemical parameters to the structural ones, three classes, encompassing each two stations, are found
linking A15 and A20 but aggregating C10 with A10 and C15 with C20 (Fig. 6c).
Few variables being too highly correlated, i.e. with a correlation greater than 0.900 (Table 4), they are
not overrepresented in the clustering analysis.
Fig. 6. Cluster analysis of the stations described by a) structural parameters alone; b) chemical
parameters alone and c) both structural and chemical parameters of the control (C) and anchoring (A)
meadow at a depth of 10,15 and 20 m. The dotted line materializes classes' separation according to
their dissimilarity.
4. Discussion
By studying both structural and chemical parameters of two seagrass meadows, one facing intensive
anchoring and the other being under no known human pressure, this study highlights the influence of
large boats anchoring on the chemistry of
Posidonia oceanica
meadows' substrate and thus, on the
seascape structure too.
4.1. An intensive anchoring for a small area?
The first step in a study of anchoring impact on seagrasses should be the analysis and characterization
of its frequency according to the size and bathymetry of the area. In the present work, the anchoring
pressure at Alga Bay, reaching 0.8 boats.ha-1.d-1 during the peak period, appears moderate compared
to previous works in Corsica (Jousseaume et al. 2013) or in Port-Cros, France witnessing up to 8.8
boats.ha-1.d-1 (Ganteaume et al. 2005a). However, anchoring pressure cannot be described by boats
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
density alone but requires in complement the proportion of boats size and their favorite substrate. In
this case, although being less numerous than small and medium boats, big ships (length > 20 m)
largely favors meadows for anchoring (84%) to sandy and rocky bottoms, leading to more important
mechanical damages at higher depths (Ganteaume et al. 2005b). It is mainly due to the fact that these
ships need deep water to anchor and that
P. oceanica
meadows are more present at these depths.
Conversely, small boats anchor on shallow sites where rocky and sandy substrates are dominant. Thus,
taking into account all these aspects, anchoring appears to be intensive in Alga Bay with a high
probability of an impact visible on the meadow structure.
4.2. From structural to chemical impact of anchoring
In this study, the analysis of the classical parameters referring to the structure of the
Posidonia
oceanica
meadow are not clearly able to depict the direct observation made by scuba diving (i.e. large
patches of bare mat crossed by anchoring tracks, Fig. 1). Here rhizomes baring and mat compactness
appear not relevant for the study of anchoring, anchors impacting the superficial part of the mat while
mat compactness investigate the whole mat thickness. This statement has already been made for mat
compactness by Milazzo et al. (2004) and Ganteaume et al. (2005a) for meadow cover and density.
Unlike these works, this case encompasses the study of big boats damages and not only the one of
small to medium ships. Thus, large ships anchoring will directly pull out whole portions of the meadow
and lead to the creation of anthropogenic patches (Fig. 7), revealed by the Conservation Index, the
meadow density, and the proportion of orthotropic/plagiotropic rhizomes. In contrast rhizomes will
not be partially uprooted and no effect will be witnessed by the rhizomes baring and mat
compactness. Thus, large ships' anchoring causes a mechanical destruction similar to the trawling one
(Boudouresque et al. 2009; Kiparissis et al. 2011 ; Pergent etal. 2013).
Another limit of the structural parameters is their incapacity to assess the impact of the substrate
change (from leafy to bare mat).
Seagrasses are known to be able to release oxygen in the sediments through their roots to create a
small oxic zone (Pedersen et al. 1998; Greve et al. 2003), this function being suppressed by the
destruction of the canopy by anchoring and thus of the photosynthesis process. These modifications
are particularly observable by studying the impact of fish farms, their action leading to large areas of
bare mats where an increase of the organic matter in decomposition leads to a decrease of the oxygen
available and the intrusion of hydrogen sulfide (Pergent-Martini et al. 2006; Holmer and Frederiksen
2007; Apostolaki et al. 2010). Although no input of organic matter - at least not in the same range as
fish farms - are involved in anchoring, the same process is observed here with a decrease of oxygen
concentration at the surface of the sediments at all depths and an intrusion of hydrogen sulfide (H2S)
inside anchoring patches. High temperatures enhancing high concentrations of H2S in
Posidonia
oceanica
meadows (Garcia et al. 2012), a decrease along with the temperature should be observed in
this case in November. In contrary, an increase in both meadows and patches is observed at the
stations where the biggest boats anchor (A15 and A20), no thermocline being observed during the two
sampling periods with an homogeneous water column of a temperature of 23.5 °C in September and
20.8 °C in November (Richir et al. 2015).
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
Fig. 7. Hypothesis on the succession of processes from mechanical damages to the expansion of
anthropogenic patches; 1 ) destruction of the canopy by anchoring, 2) fine particles deposit leading to
an increase of the organic matter and its degradation; 3 ) settlement of the alien species
Caulerpa
cylindracea;
and 4) expansion of the anchoring patch with intrusion of hydrogen sulfide (H2S).
The higher concentrations of pore water inorganic nitrate found in Alga Bay at 15 and 20 m depth
inside anchoring patches and the surrounding meadow, are another consequence of the change in
substrate. Here, the higher concentrations in ammonium (NH4+) could be the result of the particulate
organic nitrate's ammonification (Romero et al. 2006). These values constitute a sufficient nutrient
enrichment for
P. oceanica
development although recolonization does not occur (Lopez et al. 1998;
Gobert et al. 2002).
These unsuitable conditions for a recolonization by the meadow (Marbà et al. 2006), coupled with the
continuation of the high anchoring rate in the area, will thus favor the expansion of anthropogenic
patches and modify the whole sediment chemistry (Pergent-Martini et al. 2006). In this way, a new
arrangement of anthropogenic patches, possibly combined with natural ones, leads to a new seascape
(Abadie et al. 2015). The new areas of bare mat thus created are a suitable substrate for the settlement
of the alien species
Caulerpa cylindracea
Sonder (Katsanevakis et al. 2010; Kiparissis et al. 2011) which
is able to release H2S inside sediments (Garcias-Bonet et al. 2008) (Fig. 7). The so new-generated small
patches may lead to a long-term larger fragmentation of the meadow through aggregation process.
Such phenomenon has been studied in
Zostera noltii
Hornemann meadows on the Portuguese coast
by Cunha et al. (2005). In a wider viewpoint, vegetation systems, and thus seagrass seascapes, are
theoretically subject to aggregation models (Irvine et al. 2016).
4.3. The contribution of chemical parameters in seagrass meadows conservation's assessment
This study highlights the fact that using structural tools alone to assess anchoring in seagrass
meadows can lead to a misevaluation of their state of conservation. In the present work, control
stations at 15 and 20 m, meaning meadows with no traces of impact from human activities, form a
cluster, i.e. they have the same characteristics than the anchoring station at 10 m depth. It reflects no
significant anchoring impact on the meadow at this depth. Similarly, chemical features alone aggregate
a station visibly impacted by anchoring (A20) with meadows (C15 and C20) under no anthropogenic
pressures. When adding chemical parameters to the structural ones, this station is classified in the
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
same group than the control site at the same depth, reveling that no impact is observable. In the same
way stations Al5 and A20 are grouped, stating the impact of anchoring at these depths. Considering
the long term process induced by a change in sediments chemistry, the measure of several chemical
parameters can provide information about the possible recovery of a meadow under an intensive
human pressure (Holmer et al. 2008). We suspect that it will be difficult for the meadow in Alga Bay at
15 and 20 m depth to recover given the continuation of anchoring while the meadow at 10 m seems
to have the same state of conservation than the control one.
Observation of chemical modifications within seagrass meadows linked with anthropogenic impacts
has already been highlighted by Jones and Unsworth (2016) in
Zostera marina
Linnaeus across the
British Coast. This study thus reveals an excess of nitrogen within
Z. marina
leaves, associating this
observation with the poor water quality and the disturbance of boat-based activities, of which
anchoring. Chemical response of the plant to anthropogenic pressures was also stated within
Cymodocea nodosa
(Ucria) Ascherson meadows in Greece by Papathanasiou et al. (2016). These
accounts indicate that physiological and chemical changes observed within the meadows are not
confined to
P. oceanica
and the Mediterranean Sea. They are also observed in other seagrass species
with contrasted morphology and seasonal response to environmental changes, supporting the
importance of multi-disciplinary approaches for conservation assessment.
Measurement of chemical features remains however time consuming and requires specific equipment
for each element studied. In this way, new simplified protocols should be developed. Nevertheless, like
structural parameters who have already proved their utility to assess seagrasses meadow state of
conservation (Montefalcone et al. 2006; Gobert et al. 2009; Lopez y Royo et al. 2010), chemical
measures are non-destructive, have a good capacity of replication and a great potential to provide a
deeper insight (Romero et al. 2007). Moreover, these tools can be integrated in the future conservation
indices based on an ecosystemic approach in the framework of the European Marine Strategy
Framework Directive (MSFD) (Personnic et al. 2014). They also can be used in the development of
descriptors specific to anchoring, built for an easy comprehension by stakeholders and managers.
5. Conclusion
Mechanical damages of intensive anchoring in
P. oceanica
meadows induce a change in the substrate
nature leading to the generation of bare mat areas (anthropogenic patches) at 15 and 20 m depth
where the bigger ships are observed. Modifications in chemical processes, and more precisely the
intrusion of hydrogen sulfide, decrease the possibility of a recolonization by the meadow leading to
the expansion of patches. The development of non-destructive chemical indicators easy to perform,
coupled with structural tools, will provide precious information for assisting decisions in conservation
issues about mechanical impacts in seagrass meadows which, in some cases, are stoppable when
effectively assessed (Giakoumi et al. 2015a).
Acknowledgment
The authors thank Willy Champenois and Alberto V. Borges from the Chemical Oceanography Unit for
their scientific advice and participation all along the analysis process of oxygen and hydrogen sulfides,
as well as Renzo Biondo from the Laboratory of Oceanology of the University of Liège for his support
during the nutrient measurements. This study is part of the STARE-CAPMED (STAtion of Reference and
rEsearch on Change of local and global Anthropogenic Pressures on Mediterranean Ecosystems Drifts)
program funded by the Territorial Collectivity of Corsica and by The French Water Agency (PACA-
Corsica). A. Abadie acknowledges a C1FRE Ph.D. grant (2013/0470) of the French ANRT (Association
Nationale Recherche Technologie). This article is the MARE publication No. 332.
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
Appendix A. Supplementary data
Supplementary data to this article can be found online at
http://dx. doi.org/10.1016/j.marpolbul.2016.06.022.
References
Abadie, A., 2012. Evolution des herbiers à
Posidonia ocecmica
(L.) Delile dans la baie de Calvi (Corse, France) et influence de
l’ancrage dans la baie de l'Alga (Professional Master Master thesis) Aix-Marseille University, Marseille, France.
Abadie, A, Gobert, S., Bonacorsi, M., Lejeune, P., Pergent, G., Pergent-Martini, C, 2015. Marine space ecology and seagrasses.
Does patch type matter in
Posidonia ocecmica
seascapes? Ecol. Indie. 57, 435-446.
Aminot, A, Kérouel, R, 2007. Dosage automatique des nutriments dans les eaux marines Editions Quae Ifremer. Versailles,
Plouzané.
Apostolaki, E.T., Holmer, M., Marbà, N, Karakassis, I, 2010. Degrading seagrass
(Posidonia oceanica)
ecosystems: a source of
dissolved matter in the Mediterranean. Hydrobiologia 649,13-23.
Beck, M.W., Heck, K.L, Able, K.W., Childers, D.L, Eggleston, D.B., Gillanders, B.M., Halpern, B.S., Hays, C.G., Hoshino, K., Minello, T.J.,
Orth, R.J., Sheridan, P.F., Weinstein, M.P., 2001. The identification, conservation, and management of estuarine and marine
nurseries for fish and invertebrates. Bioscience 51, 633-641.
Boudouresque, C.F., Meinesz, A., 1982. Découverte de l'herbier de posidonie vol. 4. Cah. Pare nation. Port-Cros, France.
Boudouresque, C.F., Giraud, G., Panayotidis, P, 1980. Végétation marine de l’île de Port-Cros (pare National). XIX: mise en place
d'un transect permanent. Travaux Scientifiques du Pare National de Port-Cros Vol. 6, pp. 207-221.
Boudouresque, C.F., Arrighi, F., Finelli, F., Lefevre, J.R, 1995. Arrachage des faisceaux de
Posidonia oceanica
par les ancres:
protocole d'étude. Rapports Commission Internationale de la Mer Méditerranée Vol. 34, p. 21.
Boudouresque, C.F., Bernard, G., Pergent, G., Shili, A., Verlaque, M., 2009. Regression of Mediterranean seagrasses caused by
natural processes and anthropogenic disturbances and stress: a critical review. Bot. Mar. 52,395-418.
Boudouresque, C.F, Bernard, G, Bonhomme, P, Charbonnel, E., Diviacco, G., Meinesz, A, Pergent, G., Pergent-Martini, C, Ruitton, S,
Tunesi, L, 2012. Protection and conservation of
Posidonia oceanica
meadows. RAMOGE pub, Tunis.
Brooks, K.M, 2001. An evaluation of the relationship between salmon farm biomass, organic inputs to sediments,
physicochemical changes associated with those inputs and the infaunal response — with emphasis on total sediment sulfides,
total volatile solids, and oxidation-reduction potential as surrogate endpoints for biological monitoring. Aquatic Environmental
Sciences, 644 Old Eaglemount Road, Port Townsend, Washington 98368.
Calleja, M.L, Marbà, N, Duarte, CM, 2007. The relationship between seagrass
(Posidonia oceanica)
decline and sulfide porewater
concentration in carbonate sediments. Estuar. Coast. Shelf Sci. 73, 583-588.
Carpenter, J.H, 1965. The accuracy of the Winkler method for dissolved oxygen analysis. Limnol. Oceanogr. 10, 135-140.
Ceccherelli, G, Campo, D, Milazzo, M., 2007. Short-term response of the slow growing seagrass
Posidonia oceanica
to simulated
anchor impact Mar. Environ. Res. 63, 341-349.
Charbonnel, E, Boudouresque, C.F., Meinesz, A, Bernard, G, Bonhomme, P., Patrone, J, Kruczek, R, Cottalorda, J.M., Bertrandy, M.C,
Foret, P, Ragazzi, M, Le Direach, L, 2000. Le Réseau de Surveillance Posidonie de la Région Provence-Alpes-Côte d'Azur. Premiere
partie: Présentation et guide méthodologique. Année 2000. Région PACA/ Agence de l'Eau RMC/GIS Posidonie/CQEL 13/CQEL
83/Conseil Général 6, Marseille, France.
Costanza, R, d'Arge, R, de Groot, R, Farber, S, Grasso, M, Hannon, B, Limburg, K, Naeem, S, O'Neill, R.V, Paruelo, J, Raskin, RG,
Sutton, P, van den Belt, M, 1997. The value of the world's ecosystem services and natural capital. Nature 387,253-260.
Cullen-Unsworth, L, Unsworth, R, 2013. Seagrass meadows, ecosystem services, and sustainability. Environ. Sci. Policy Sustain.
Dev. 55,14-28.
Cunha, A.H, Santos, R.P., Caspar, A.P, Bairros, M.F, 2005. Seagrass landscape-scale changes in response to disturbance created by
the dynamics of barrier-islands: a case study from Ria Formosa (Southern Portugal). Estuar. Coast Shelf Sci. 64,636-644.
Fourqurean, J.W., Duarte, CM., Kennedy, H., Marba, N., Holmer, M, Mateo, MA, Apostolaki, E.T., Kendrick, GA, Krause-Jensen, D,
McGlathery, K.J, Serrano, O, 2012. Seagrass ecosystems as a globally significant carbon stock. Nat. Geosci. 5, 505-509.
Francour, P., Ganteaume, A, Poulain, M., 1999. Effects of boat anchoring in
Posidonia oceanica
seagrass beds in the Port-Cros
National Park (North-Western Mediterranean Sea). Aquat Conserv. Mar. Freshwat. Ecosyst 9, 391-400.
Ganteaume, A., Bonhomme, P., Bernard, G., Poulain, M, Boudouresque, C.F., 2005a. Impact de l'ancrage des bateaux de plaisance
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
sur la prairie à
Posidonia oceanica
dans le Pare national de Port-Cros (Méditerranée nord-occidentale). Sci. Rep. Port-Cros Natl.
Park 21,147-162.
Ganteaume, A., Bonhomme, P., Emery, E., Hervé, G., Boudouresque, C.F., 2005b. Impact sur la prairie à
Posidonia oceanica
de
l'amarrage des bateaux de croisière, au large du port de Porquerolles (Provence, France, Méditerranée). Sci. Rep. Port-Cros Natl.
Park 21, 163-173.
García, R., Sánchez-Camacho, M., Duarte, C.M., Marbà, N, 2012. Warming enhances sulphide stress of Mediterranean seagrass
(Posidonia oceanica).
Estuar. Coast Shelf Sci. 113, 240-247.
Garrias-Bonet, N, Marba, N, Holmer, M, Duarte, CM, 2008. Effects of sediment sulfides on seagrass
Posidonia oceanica
meristematic activity. Mar. Ecol. Prog. Ser. 372,1-6.
Giakoumi, S, Sini, M, Gerovasileiou, V, Mazor, T., Beher, J, Possingham, H.P., Abdulla, A, Çinar, M.E, Dendrinos, P., Gucu, A.C.,
Karamanlidis, A.A., Rodic, P, Panayotidis, P., Taskin, E, Jaldin, A., Voultsiadou, E., Webster, C., Zenetos, A, Katsanevakis, S., 2013.
Ecoregion-based conservation planning in the Mediterranean: dealing with large-scale heterogeneity. PLoS One 8, e76449.
Giakoumi, S., Brown, C.J., Katsanevakis, S, Saunders, M.I., Possingham, H.P., 2015a. Using threat maps for cost-effective
prioritization of actions to conserve coastal habitats. Mar. Policy 61, 95-102.
Giakoumi, S., Halpern, B.S., Michel, L.N., Gobert, S, Sini, M, Boudouresque, C.F., Gambi, M.C, Katsanevakis, S, Lejeune, P,
Montefalcone, M, Pergent, G, Pergent-Martini, C, Sanchez-Jerez, P, Velimirov, B, Vizzini, S, Abadie, A., Coll, M, Guidetti, P., Micheli,
F, Possingham, H.P, 2015b. Towards a framework for assessment and management of cumulative human impacts on marine food
webs. Conserv. Biol. 29,1228-1234
Gobert, S, Laumont, N, Bouquegneau, J.M, 2002.
Posidonia oceanica
meadow: a low nutrient high chlorophyll (LNHC) system?
BMC Ecol. 2,9.
Gobert, S, Lepoint, G, Biondo, R, Bouquegneau, J.M, 2006.
In situ
sampling of pore waters from seagrass meadows. Biol. Mar.
Mediterr. 13, 230-234.
Gobert, S, Sartoretto, S, Rico-Raimondino, V, Andral, B, Chery, A., Lejeune, P, Boissery, P., 2009. Assessment of the ecological
status of Mediterranean French coastal waters as required by the Water Framework Directive using the
Posidonia oceanica
Rapid
Easy Index: PREI. Mar. Pollut Bull. 58, 1727-1733.
Gravez, V, Gelin, A, Charbonnel, E, Francour, P., Abellard, O., Remonnay, O., 1995. Surveillance de l'herbier de Posidonie de la baie
du Prado (Marseille) - Suivi 1995.
Grech, A., Chartrand-Miller, K., Erftemeijer, P.L.A., Fonseca, M.S, McKenzie, L, Rasheed, M, Taylor, H, Coles, R, 2012. A comparison
of threats, vulnerabilities and management approaches in global seagrass bioregions. Environ. Res. Lett 7, 024006.
Greve, T.M., Borum, J., Pedersen, O., 2003. Meristematic oxygen variability in eelgrass
(Zostera marina).
Limnol. Oceanogr. 48,
210-216.
Halpern, B.S, Walbridge, S, Selkoe, KA, Kappel, C.V., Micheli, F, D'Agrosa, C, Bruno, J.F., Casey, K.S, Ebert, C, Fox, H.E, Fujita, R,
Heinemann, D, Lenihan, H.S, Madin, E.M.P, Perry, M.T, Selig, E.R, Spalding, M, Steneck, R, Watson, R, 2008. A global map of
human impact on marine ecosystems. Science (Washington, DC) 319, 948-952.
Holmer, M, Frederiksen, M.S, 2007. Stimulation of sulfate reduction rates in Mediterranean fish farm sediments inhabited by the
seagrass
Posidonia oceanica.
Biogeochem-istry (Dordrecht) 85,169-184.
Holmer, M., Duarte, C.M., Marbá, N., 2003. Sulfur cycling and seagrass
(Posidonia oceanica)
status in carbonate sediments.
Biogeochemistry 66, 223-239.
Holmer, M., Argyrou, M., Dalsgaard, T., Danovaro, R., Diaz-Almela, E, Duarte, CM, Frederiksen, M, Grau, A, Karakassis, I, Marbà, N,
Mirto, S, Perez, M, Pusceddu, A, Tsapakis, M, 2008. Effects offish farm waste on
Posidonia oceanica
meadows: synthesis and
provision of monitoring and management tools. Mar. Pollut. Bull. 56, 1618-1629.
Holon, F, Mouquet, N, Boissery, P, Bouchoucha, M, Delaruelle, G, Tribot, A.S, Deter, J, 2015. Fine-scale cartography of human
impacts along French Mediterranean coasts: a relevant map for the management of marine ecosystems. PLoS One 10, e0135473.
Irvine, MA, Bull, J.C, Keeling, M.J, 2016. Aggregation dynamics explain vegetation patch-size distributions. Theor. Popul. Biol. 108,
70-74.
Jones, B.L, Unsworth, RK.F, 2016. The perilous state of seagrass in the British Isles. R Soc. Open Sci. 3.
Jorda, G, Marba, N, Duarte, CM, 2012. Mediterranean seagrass vulnerable to regional climate warming. Nat. Clim. Chang. 2, 821-
824.
Jousseaume, M, Buron, K, Chery, A, Lejeune, P, 2013. Etude relative à la plaisance et aux mouillages en Corse: Rapport final -
Année 2012/2013. STARESO, Calvi, Corsica.
Katsanevakis, S, Issaris, Y, Poursanidis, D, Thessalou-Legaki, M, 2010. Vulnerability of marine habitats to the invasive green alga
Caulerpa racemosa
var.
cylindracea
within a marine protected area. Mar. Environ. Res. 70,210-218.
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
Kiparissis, S, Fakiris, E, Papatheodorou, G., Geraga, M, Kornaros, M, Kapareliotis, A, Ferentinos, G., 2011. Illegal trawling and
induced invasive algal spread as collaborative factors in a
Posidonia oceanica
meadow degradation. Biol. Invasions 13, 669-678.
Lopez y Royo, C., Casazza, G., Pergent-Martini, C., Pergent, G., 2010. A biotic index using the seagrass
Posidonia oceanica
(BiPo),
to evaluate ecological status of coastal waters. Ecol. Indie. 10, 380-389.
López, N.I, Duarte, CM, Vallespinós, F, Romero, J, Alcoverro, T, 1998. The effect of nutrient additions on bacterial activity in
seagrass
(Posidonia oceanica)
sediments. J. Exp. Mar. Biol. Ecol. 224, 155-166.
Marbà, N, Holmer, M, Gacia, E, Barron, C, 2006. Seagrass beds and coastal biogeochemistry. In: Larkum, A.W.D, Orth, R.J., Duarte,
C.M. (Eds.), Seagrasses: Biology, Ecology and Conservation. Springer.
Mateo, MA, Romero, J, 1997. Detritus dynamics in the seagrass
Posidonia oceanica:
elements for an ecosystem carbon and
nutrient budget Mar. Ecol. Prog. Ser. 151,43-53.
Michel, L, Abadie, A, Biondo, R, Borges, A, Collignon, A, Champenois, W, Chery, A, Donnay, A, Gobert, S, Goffart, A, Hecq, J.-H,
Pelaprat, C, Pere, A, Plaza, S, Thome, J.-P, Volpon, A, Lejeune, P, 2012. STARE-CAPMED - Rapport d'activité 2012. STARESO.
Milazzo, M, Badalamenti, F, Ceccherelli, G, Chemello, R, 2004. Boat anchoring on
Posidonia oceanica
beds in a marine protected
area (Italy, western Mediterranean): effect of anchor types in different anchoring stages. J. Exp. Mar. Biol. Ecol. 299, 51-62.
Montefalcone, M, Albertelli, G, Bianchi, CN, Mariani, M, Morri, C, 2006. A new synthetic index and a protocol for monitoring the
status of
Posidonia oceanica
meadows : a case study at sanremo (Ligurian Sea, NW Mediterranean). Aquat Conserv. Mar.
Freshwat Ecosyst. 16, 29-42.
Moreno, D, Aguilera, PA, Castro, H, 2001. Assessment of the conservation status of seagrass
(Posidonia oceanica)
meadows:
implications for monitoring strategy and the decision-making process. Biol. Conserv. 102, 325-332.
Ondiviela, B, Losada, I.J, Lara, J.L, Maza, M, Galván, C, Bouma, T.J, van Belzen.J, 2014. The role of seagrasses in coastal protection
in a changing climate. Coast. Eng. 87, 158-168.
Papathanasiou, V, Orfanidis, S, Brown, M.T., 2016.
Cymodocea nodosa
metrics as bioindicators of anthropogenic stress in N.
Aegean, Greek coastal waters. Ecol. Indie. 63,61-70.
Pedersen, M.O., Borum, J., Duarte, C.M., Fortes, M.D., 1998. Oxygen dynamics in the rhizo-sphere of
Cymodocea rotundata.
Mar.
Ecol. Prog. Ser. 169, 283-288.
Pergent, G., Pergent-Martini, C., Boudouresque, C.F., 2013. Trawling impacts on Mediterranean seagrass. Seagrass-Watch 26-30.
Pergent-Martini, C, Leoni, V., Pasqualini, V., Ardizzone, G.D., Balestri, E., Bedini, R, Belluscio, A., Belsher, T., Borg, J., Boudouresque,
C.F, Boumaza, S., Bouquegneau, J.-M, Buia, M.C., Calvo, S, Cebrian, J, Charbonnel, E, Cinelli, F., Cossu, A, Di Maida, G, Dural, B.,
Francour, P., Gobert, S., Lepoint, G., Meinesz, A., Molenaar, H., Mansour, H.M., Panayotidis, P., Peirano, A., Pergent, G., P iazzi, L.,
Pirrotta, M., Relini, G., Romero, J., Sanchez-Lizaso, J.L., Semroud, R, Shembri, P., Shili, A., Tomasello, A, Velimirov, B, 2005.
Descriptors
of Posidonia ocecmica
meadows: use and application. Ecol. Indie. 5,213-230.
Pergent-Martini, C, Boudouresque, C.F., Pasqualini, V., Pergent, G., 2006. Impact of fish farming facilities on
Posidonia ocecmica
meadows: a review. Mar. Ecol. 27, 310-319.
Personnic, S, Boudouresque, C.F., Astruch, P, Ballesteros, E., Blouet, S, Bellan-Santini, D, Bonhomme, P., Thibault-Botha, D.,
Feunteun, E., Harmelin-Vivien, M., Pergent, G., Pergent-Martini, C, Pastor, J., Poggiale, J.C., Renaud, F., Thibaut, T., Ruitton, S.,
2014. An ecosystem-based approach to assess the status of a mediterranean ecosystem, the
Posidonia oceanica
seagrass
meadow. PLoS One 9, e98994.
Richir, J., Abadie, A., Binard, M., Biondo, R, Borges, A., Cimiterra, N., Collignon, A., Champenois, W., Donnay, A., Fréjefond, C,
Gobert, S., Goffart, A., Lepoint, G., Pelaprat, C, Pere, A., Sirjacobs, D., Thome, J.P., Volpon, A, Lejeune, P., 2015. STARE-CAPMED -
Rapport d'activité 2014. STARESO, Calvi, France.
Romero, J., Lee, K.-S., Perez, M., Mateo, M.A., Alcoverro, T., 2006. Nutrient dynamics in seagrass ecosystems. In: Larkum, AW.D.,
Orth, R.J, Duarte, CM. (Eds.), Seagrasses: Biology, Ecology and Conservation, Book 1. Springer.
Romero, J, Martinez-Crego, B., Alcoverro, T., Perez, M., 2007. A multivariate index based on the seagrass
Posidonia oceanica
(POMI) to assess ecological status of coastal waters under the water framework directive ( WFD). Mar. Pollut Bull. 55, 196-204.
Ruiz, J.M., Boudouresque, C.F, Enriquez, S., 2009. Mediterranean seagrasses. Bot Mar. 52, 369-381.
Short, F., Carruthers, T., Dennison, W., Waycott, M., 2007. Global seagrass distribution and diversity: a bioregional model. J. Exp.
Mar. Biol. Ecol. 350,3-20.
Strickland, J.D.H., Parsons, T.R, 1972. A Practical Handbook of Seawater Analysis. Fisheries Research Board of Canada, p. 328.
UNEP-MAP-RAC/SPA 2011. Draft guidelines for the standardization of mapping and monitoring methods of marine
magnoliophyta in the Mediterranean. Working Document, Prepared by C Pergent-Martini for the Tenth Meeting of Focal Points
for SPAs. Book UNEP(DEPI)/MED WG 359/9. RAC/SPA Publ., Marseille, France.
Published in: Marine Pollution Bulletin (2016)
Status: Postprint (author’s version)
Vassallo, P., Paoli, C, Rovere, A, Montefalcone, M, Morri, C, Bianchi, C.N., 2013. The value of the seagrass
Posidonia oceanica:
a
natural capital assessment Mar. Pollut Bull. 75, 157-167.
Winkler, L.K.W., 1888. Die Bestimmung des in Wasser gelösten Sauerstoffs. Ber. Deut. Chem. Ges. 21,2843-2855.
