Marine Pollution Bulletin 106 (2016) 162–173

Contents lists available at ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Long-term fluctuations in Cystoseira populations along the west Istrian

Coast (Croatia) related to eutrophication patterns in the northern
Adriatic Sea
Ljiljana Iveša ⁎, Tamara Djakovac, Massimo Devescovi
Ruđer Bošković Institute, Center for Marine Research, G. Paliaga 5, 52210 Rovinj, Croatia

a r t i c l e i n f o a b s t r a c t

Article history: An exploration of historical data suggested that eutrophication patterns might drive long-term fluctuations in
Received 23 November 2015 Cystoseira populations along the west Istrian Coast (northern Adriatic Sea, Croatia). The regimes of northern Ital-
Received in revised form 3 March 2016 ian rivers, which flow approximately 100 km west of the study area, mainly modulate the eutrophication levels of
Accepted 6 March 2016
the northern Adriatic Sea. A regression of Cystoseira populations from the 1970s through the 1990s corresponded
Available online 12 March 2016
to increased levels of eutrophication in the study area. During the late 1990s, the density of sea urchins, which are
Keywords:
efficacious macroalgal predators, decreased, likely due to an intense formation of pelagic mucilage aggregates
Cystoseira that resulted in mass mortality episodes of macrozoobenthic species. During the 2000–2013 period, an
Long-term changes oligotrophication of the northern Adriatic formed the basis for the recovery of Cystoseira taxa, whose abundances
Eutrophication from 2009 to 2013 were similar to those characterising the most flourishing Mediterranean Cystoseira
Sea urchins assemblages.
Pelagic mucilage © 2016 Elsevier Ltd. All rights reserved.
Northern Adriatic Sea

1. Introduction not included because it can withstand intermediate levels of pollution

The canopy-forming macroalgae that compose marine forests are
clearly declining at local, regional and global scales at an alarming rate
(Airoldi and Beck, 2007; Steneck et al., 2002; Connell et al., 2008; Kang
et al., 2008). Cystoseira species (Phaeophyceae, Fucales) are large,
canopy-forming brown macroalgae, and they are able to form dense
belts or forests on the rocky substrate of the Mediterranean Sea that ex-
tend from the upper level of the sublittoral to the upper circalittoral
zone (Giaccone and Bruni, 1973). Their distribution is usually strictly de-
pendent on depth and the intensity of the wave action (Sauvageau, 1912;
Feldmann, 1937; Ercegović, 1952; Molinier, 1960; Verlaque, 1987;
Ballesteros, 1988, 1990; Giaccone et al., 1994; Cormaci, 1995), and as hab-
itat engineers (sensu Jones et al., 1994), Cystoseira species shelter numer-
ous organisms and thus play an important role in sustaining the
biodiversity of Mediterranean coastal ecosystems (Molinier, 1960;
Ballesteros et al., 1998, 2009; Pitacco et al., 2014). However, Cystoseira
species are particularly sensitive to anthropogenic pressures, so all
Mediterranean species, except Cystoseira compressa (Esper) Gerloff and
Nizamuddin subsp. compressa (Thibaut et al., 2015), are listed as
protected species in Annex II on the List of Endangered or Threatened
Species (UNEP-PAM-RAC/SPA, 2012); C. compressa subsp. compressa is
⁎ Corresponding author.
E-mail address: ivesa@cim.irb.hr (L. Iveša).
(Soltan et al., 2001; Mangialajo et al., 2008; Pinedo et al., 2013; Thibaut
et al., 2014). Although Cystoseira species are listed as threatened in inter-
national conventions, they are not effectively protected (Thibaut et al.,
2015). Furthermore, Cystoseira species have been successfully used as
ecological indicators of pristine environments (Orfanidis et al., 2003;
Ballesteros et al., 2007; Asnaghi et al., 2009; Bermejo et al., 2013;
Nikolić et al., 2013) for the implementation of the Water Framework Di-
rective (EC, 2000).
In addition to anthropogenic pressures, global warming (Harley
et al., 2012; Mineur et al., 2015), overgrazing by herbivores (Hereu,
2006; Guidetti, 2006; Vergés et al., 2009; Gianguzza et al., 2011;
Bianchi et al., 2014; Vergés et al., 2014) and physical sea conditions,
such as extreme storms (Navarro et al., 2011) and prolonged low tides
(Rodrìguez-Prieto, 1992), negatively affect Cystoseira populations. An-
thropogenic impacts can act at local or larger spatial scales. Sewage dis-
charge and urban pollution degrade Cystoseira populations at a
restricted spatial scale (Munda, 1980a, 1982; Soltan et al., 2001;
Perkol-Finkel and Airoldi, 2010; Sales et al., 2011; Thibaut et al., 2014;
Pinedo et al., 2015), and further examples of local impacts include in-
creased grazing by herbivores due to overfishing of sea urchin predators
(Sala et al., 1998; Guidetti and Sala, 2007) and the deleterious effects of
harvesting date mussels (Guidetti et al., 2003). However, larger-scale
phenomena, due to anthropogenic influences on patterns of pelagic eu-
trophication, might also affect Cystoseira demography. The extinction of
some Cystoseira species along the coasts of the Tremiti Archipelago

http://dx.doi.org/10.1016/j.marpolbul.2016.03.010
0025-326X/© 2016 Elsevier Ltd. All rights reserved.
 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173
(central Adriatic Sea, Italy) was related to a reduction in water transpar-
ency, and as the archipelago was not subjected to local pollution
(Cormaci and Furnari, 1999), the observed increase in turbidity could
be due to fluctuations in offshore eutrophication.
The northern Adriatic is the northernmost biogeographic sector of
the Mediterranean Sea (Bianchi and Morri, 2000). It is a shallow (max-
imum depth of approximately 50 m) and semi-enclosed basin
characterised by seawater temperatures below 11 °C in February
(Bianchi, 2007). The runoff regimes of northern Italian rivers, which dis-
charge their waters approximately 100 km from the west Istrian Coast,
play a pivotal role in short-term and long-term variations in the eutro-
phication levels of the northern Adriatic Sea (Degobbis et al., 2000;
Djakovac et al., 2012, 2015). On its west and north sides, the northern
Adriatic biogeographic sector encompasses the predominantly sandy
Italian Coast from Ancona to Trieste, and the west coast of the Istrian
Peninsula delimits its eastern border. Along this coast, the sea bottom
is mainly rocky up to a depth of approximately 12 m, so it is particularly
suitable for the formation of large Cystoseira forests. Comprehensive his-
torical data on the distribution of Cystoseira species along the west
Istrian Coast date back to 1950 (Ercegović, 1952), and subsequent stud-
ies have provided additional information on their distribution patterns
(Munda, 1979, 1980a, 1980b, 1982; Hanel, 2002).
Of the approximately 40 Mediterranean Cystoseira taxa (Ribera et al.,
1992; Gómez Garreta et al., 2001; Draisma et al., 2010; Cormaci et al.,
2012; Guiry and Guiry, 2015), only eight dwell along the west Istrian
Coast (Ercegović, 1952). These eight taxa can be considered euryther-
mic because they can be found across the whole Mediterranean Sea
and are capable of withstanding the cold winter seawater temperatures
characteristic for the northern Adriatic Sea (Ercegović, 1952). The eight
taxa are:
(1) Cystoseira amentacea var. stricta Montagne; described as
Cystoseira spicata spec. nov. in Ercegović (1952) and referred to
as C. amentacea in the following text;
(2) Cystoseira barbata (Stackhouse) C. Agardh f. barbata (Thibaut
et al., 2015); described as C. barbata J. Agardh in Ercegović
(1952) and referred to as C. barbata in the following text;
(3) C. compressa (Esper) Gerloff & Nizamuddin subsp. compressa
(Thibaut et al., 2015); described as Cystoseira abrotanifolia C.
Agardh in Ercegović (1952) and referred to as C. c. compressa in
the following text;
(4) C. compressa subsp. pustulata (Ercegović) Verlaque comb. nov.
(Thibaut et al., 2015); described as C. abrotanifolia subs. pustulata
subs. nov. Ercegović in Ercegović (1952) and referred to as C. c.
pustulata in the following text;
(5) Cystoseira corniculata (Turner) Zanardini; described as
C. corniculata Hauck in Ercegović (1952);
(6) Cystoseira crinita Duby; described as C. crinita Bory in Ercegović
(1952);
(7) Cystoseira foeniculacea f. schiffneri (Hamel) Gómez Garreta,
Barceló, Ribera & Rull Lluch; described as Cystoseira discors C.
Agardh in Ercegović (1952) and referred to as C. foeniculacea in
the following text;
(8) Cystoseira spinosa var. spinosa Sauvageau; described as Cystoseira
adriatica Sauvageau in Ercegović (1952) and referred to as
C. spinosa in the following text.
Among these eight taxa, only C. amentacea is able to dwell in the
upper level of the sublittoral zone, where it forms dense belts, but along
the eastern coast of the Adriatic Sea, sparse thalli of C. amentacea can be
found up to a depth of 2–3 m. The alga exclusively colonises habitats
that are exposed to wave action with very low sedimentation rates but
is rare in areas subject to extreme wave action; such habitats are usually
devoid of Cystoseira species (Ercegović, 1952). C. crinita forms belts from
immediately below the upper level of the sublittoral zone to 3 m in depth
in habitats that are sheltered and intermediately exposed to wave action;
163
the species is less sensitive to sedimentation than C. amentacea. The re-
maining six taxa are found in the eastern Adriatic Sea from immediately
below the upper level of the sublittoral zone to approximately 40 m in
depth, except C. foeniculacea, which was sampled up to 110 m in depth
(Ercegović, 1952). Of these six taxa, only C. barbata, C. crinita, and C. c.
compressa form dense forests at shallow depths (from 0.5 to 3 m), and
all six are adapted to dwell in habitats with intermediate levels of sedi-
mentation. At shallow depths, they are present in habitats that are inter-
mediately exposed to wave action, with two exceptions. First, C. barbata
is widespread but exclusively found in very sheltered habitats, and sec-
ond, C. c. compressa can colonise very exposed as well as very sheltered
habitats. In habitats that are highly exposed to wave action, the thalli of
C. c. compressa have a flattened form, which Ercegović (1952) termed “ro-
setta”. In habitats that are very sheltered from wave action, C. c. compressa
thalli are very vertically developed, attaining a total thallus height of
more than 0.5 m, which, in the eastern Adriatic Sea, can only be compared
to the height of C. barbata thalli (Ercegović, 1952).
The aim of this study is to investigate whether long-term variations
in Cystoseira populations along the west Istrian Coast have developed in
relation to the changes in eutrophication levels occurring in the pelagic
region of the northern Adriatic Sea. First, to estimate the status of
Cystoseira populations along the west Istrian Coast, we compared re-
cently assessed abundance values with those reported for other, less im-
pacted Mediterranean regions. Second, we evaluated if the regression-
recovery phases of Cystoseira populations reflect long-term variations
in eutrophication levels. Finally, we examined whether historical varia-
tions in the abundance of sea urchins, which are generally recognised as
major macroalgal grazers (Sala et al., 1998), are related to the pelagic
mucilage phenomenon. Mucilage aggregates formed episodically in
the water column of the northern Adriatic Sea during the 19th and
20th centuries (Degobbis et al., 1995, 2000), provoking mass mortality
events of macrozoobenthic organisms (Stachowitsch et al., 1990;
Müller et al., 1998).
2. Materials and methods
2.1. Study area and historical data
The west Istrian Coast (Fig. 1) extends from Cape Savudrija in the
north to Cape Kamenjak in the south. The length of the coastline totals
439 km, and the islands contribute an additional 89 km, according to a
1:5000-scale map (source: Institute for Physical Planning — Region of
Istria). Floristic data on Cystoseira taxa for the study area dating back
to the 19th century were collected from Kuckuck's field diaries (revised
by Munda, 2000) and the herbarium collection of the Center for Marine
Research in Rovinj (results reported in the Supplementary material).
However, more comprehensive data for the study area were found in
Ercegović (1952) and Munda (1980a, 1980b, 1982, 2000), and historical
data on sea urchin distributions are from Munda (1982); Hanel (2002)
and Guidetti and Dulčić (2007). Information on the occurrence of the
mucilage phenomenon in the water column of the northern Adriatic
Sea came from the Database of the Center for Marine Research in Rovinj
(Croatia).
2.2. Eutrophication levels
The eutrophication levels in the study area were characterised as the
concentrations of chlorophyll a, orthophosphate and nitrate, which were
measured at an oceanographic station (Station RV001, 45° 4ʹ 48ʺ N; 13°
36ʹ 36ʺ E) located several nautical miles from the city of Rovinj (Fig. 1).
Station RV001 is part of a system of 7 stations that encompasses the en-
tire northern Adriatic from the Rovinj region to Italian waters in the prox-
imity of the Po River delta, and long-term studies demonstrate that data
from Station RV001 reflect the eutrophication fluctuations of the entire
basin (Degobbis et al., 2000; Djakovac et al., 2012). The concentration of
chlorophyll a was measured fluorometrically after extraction with
164 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173

Fig. 1. A map of the west Istrian Coast with sampling areas (Novigrad = N, Vrsar = V and Rovinj = R) and nested sampling stations. The cross indicates the RV001 oceanographic station
near the city of Rovinj. The Longa Island and St. Katarina Island stations surveyed by Ercegović (1952) are indicated as E1 and E2, respectively.

acetone through Whatman GF/C filters (Strickland and Parsons, 1972),
and the concentrations of orthophosphate and nitrate were determined
by standard spectrophotometric methods (Strickland and Parsons,
1972). Seawater samples were collected using Niskin bottles at 5 depths
(0, 5, 10, 20 and 27 m, i.e., 2 m above the sea bottom), and measurements
were performed approximately monthly during the period 1974–2013.
Data were explored as the arithmetic mean ± SEM for 3 periods:
(1) from 1974 to 1988, (2) from 1989 to 1999 and (3) from 2000 to
2013; these subdivisions were chosen because a period of intense plank-
tonic mucilage aggregate formation began in the northern Adriatic Sea in
1989 (Degobbis et al., 1999). In the early 2000s, the northern Adriatic en-
tered a phase of oligotrophication (Djakovac et al., 2012; Giani et al.,
2012), so 2000 was chosen as the first year for the final period. Within
each period, data were subdivided into 2 times of the year, March–August
and September–February, corresponding to the phases of intensive
growth and quiescence of Cystoseira species, respectively (Ercegović,
1952).
stations sampled by Ercegović (1952) in 1950 (Longa Island, in the
Vrsar area: 45° 8ʹ 34ʺ N, 13° 34ʹ 50ʺ E and St. Katarina Island, located at
the entrance of the port of Rovinj: 45° 4ʹ 39ʺ N, 13° 37ʹ 30ʺ E) were sur-
veyed during 2010–2013. These stations (Fig. 1) were considered because
they represent the northernmost historically recorded settlements of
C. amentacea on the west Istrian Coast.
The same methodology was used to estimate the extent of sea urchin
barrens, which were usually distributed along rocky bottoms from
depths of approximately 1 m to several metres. For each sea urchin bar-
ren within a sector, the two points representing either end of the barren
were projected orthogonally on the coastline, and the extent was
expressed as a percentage of the length of the coastline. In addition,
three 1 × 1 m quadrates were randomly placed within the sea urchin
barrens, and the abundances of Arbacia lixula (Linnaeus, 1758) and
Paracentrotus lividus (Lamarck, 1816) were recorded in situ.
2.4. Subtidal Cystoseira sampling

2.3. Visual assessment of C. amentacea and sea urchins
The distribution of C. amentacea along the upper level of the sublittoral
of the west Istrian Coast was visually assessed by following the coast with
a small boat in spring during the 2010–2013 period. The mapping was
performed along 19 sectors, which amounted to 150 km of the west
Istrian coastline. The length of the coastline occupied by C. amentacea
was assessed within each sector, and the abundance of the species was
expressed as a percentage of the length of the coastline. Additionally, 2
In April 2009, Cystoseira taxa were sampled along the west Istrian
Coast according to a hierarchical sampling design. Three areas were ran-
domly selected (Novigrad = N, Vrsar = V and Rovinj = R; Fig. 1) that
were located several tens of kilometres from each other and at least
3 km from sources of local pollution (sewage outlets, urban areas and
tourism resorts). Thus, we assumed that the effects of local pollution
on Cystoseira species might be excluded, and only the gently sloping
rocky bottom along the coast, which is intermediately exposed to
wave action, was sampled. Within each sampling area, three stations
 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173 165

located several kilometres apart were randomly chosen (Fig. 1), and at
each station, 3 approximately 10 × 10 m plots spaced several tens of
metres from each other were chosen at random. Three 50 × 50 cm
quadrates were randomly placed in each plot, and all of the Cystoseira
species present within each quadrat were collected using a hammer
and chisel. The same procedure was repeated at 3 depth ranges: from
0.5 to 2, from 5 to 7 and from 10 to 12 m. After collection, samples
were transported to the laboratory in plastic bags, and species were
identified according to Ercegović (1952) and Gómez Garreta et al.
(2001). Current species names followed Thibaut et al. (2015) and
Guiry and Guiry (2015). After absorbing the residual seawater with fil-
ter paper, the wet weight of each species in each sample was deter-
mined. Additionally, all of the sampling stations were surveyed each
year during spring from 2010 to 2013 to ascertain if any relevant chang-
es in the extent of the Cystoseira forest and sea urchin density had
occurred.
Data were subjected to permutational multiple analysis of variance
(PERMANOVA), non-metric multidimensional scaling (MDS) and clus-
ter ordination using the software package PERMANOVA+ for PRIMER
(PRIMER-E, Plymouth, UK).
The status of each taxon during each of these three historical periods
was compared to the quantitative assessments performed in this
study during the period 2009–2013, and additional historical data
confirming long-term fluctuations in Cystoseira taxa are provided in
Table 1. However, it should be emphasised that Cystoseira did not
completely disappear from the west Istrian Coast during the 1978–
1997 regression phase; species persisted in refuges, such as rocky
pools (Munda, 1982), and in the subtidal of several locations in the
study area, such as Cape Savudrija (45° 30ʹ 10ʺ N, 13° 30ʹ 59ʺ E), Faborso
Bay (45° 7ʹ 9ʺ N, 13° 36ʹ 53ʺ E) and Korente Point (45° 3ʹ 48ʺ N, 13° 37ʹ
45ʺ E) (Babbini, 1991). All of the Cystoseira taxa recorded by Ercegović
in 1950 can be considered as being very common in the study area
from 2009 to 2013 (Table 1).
Long-term fluctuations in sea urchin density showed an opposite
trend to that of the Cystoseira taxa; they were rare during the 1950–
1974 period and very common during the 1978–1997 period. Contrast-
ing results were reported in the literature for the period 1999–2004.
During the period 2009–2013, they can be considered as rare along
the entirety of the west Istrian Coast (Table 1). However, increased
sea urchin densities were observed in the south part of the west Istrian
Coast from a depth of approximately 1 m to several metres (Fig. 2B).

3. Results
3.1. Historical data
The historical data on the distributions of Cystoseira taxa and sea ur-
chins along the west Istrian Coast were subdivided into three periods
(Table 1). The first period was from 1950, when Ercegović (1952) ex-
haustively assessed the distribution of Cystoseira taxa in the study
area, to 1974, the last description of well-developed Cystoseira forests
in the Rovinj region (Munda, 1979, 2000). The second period was
from 1978, when Munda (1980a, 1980b) detected significant degrada-
tion of the Cystoseira forests in the region of Rovinj, to 1997, when
Hanel (2002) observed low Cystoseira species cover in the same study
area. The third period lasted from 1999, when a substantial recovery
of Cystoseira forest was recorded (Hanel, 2002), to 2004, when the last
Cystoseira forest surveys were conducted (Devescovi and Iveša, 2007).
3.2. The mucilage phenomenon
Since 1986, the northern Adriatic has experienced the summer for-
mation of mucilage aggregates (Fig. 3), whose dimensions range from
a few centimetres up to several metres. However, the most characteris-
tic forms are the voluminous aggregates with diameters of several me-
tres and less massive aggregates in the form of strings or ribbons that
can reach several metres in length (Precali et al., 2005). Two major pe-
riods of mucilage formation can be distinguished (Fig. 3). From 1986 to
1991, there were two ribbon formation events and three events
characterised by the formation of voluminous aggregates, and the phe-
nomenon was particularly intense in 1989. The second period of volu-
minous mucilage aggregate formation occurred from 1997 to 2004,
but since then, only mild mucilage events have been observed, whose
aggregates were mostly in the form of strings and ribbons.

Table 1
Summary of historical distribution data of Cystoseira macroalgae and sea urchins along the western Istrian Coast.

Cystoseira species 1950–1974 1978–1997 1999–2004 2009–2013 (This study)

(1) C. amentacea var. stricta Very common (a, d) Rare (e) Not found (g, h) Very common
Common (c) Common (f)
(2) C. barbata f. barbata Very common (a, c, d) Very rare (e) Very common (g) Very common
Common (b) Common (f) Common (h)
(3) C. compressa subsp. compressa Very common (a, d) Very rare (e, f) Very common (g, h) Very common
Common (b, c)
(4) C. compressa subsp. pustulata Very common (a) Not found (e, f) Not found (g, h) Very common
(5) C. crinita Very common (a, d) Not found (e, f) Not found (g) Very common
Common (c) Common (h)
(6) C. corniculata Very common (a) Very rare (e) Not found (g) Very common
Rare (c) Not found (f) Rare (h)
(7) C. foeniculacea f. schiffneri Very common (a, c, d) Not found (e, f) Not found (g) Very common
Rare (g)
(8) C. spinosa var. spinosa Very common (a, d) Very rare (e) Not found (g, h) Very common
Common (c) Not found (e)
As Cystoseira forests⁎ Well developed (d) Reduced (i) Recovering (i) Well developed

Sea urchins
Arbacia lixula Rare (e) Very common (i, e) Common (i) Rare
Not found (j)
Paracentrotus lividus Rare (e) Very common (i, e) Common (i) Rare
Rare (j)

Sampling area and time: (a) West Istrian Coast in 1950 (Ercegović, 1952). (b) Islands of the Rovinj area during 1964–1974 (Seneš, 1989). (c) Rovinj area during 1967–1970 (Munda, 1972,
1979; Munda, 2000). (d) West Istrian Coast during 1963–1968 (Špan, 1969). (e) Rovinj area during 1978–1983 (Munda, 1980a, 1980b, 1982, 1993, 2000). (f) West Istrian Coast in 1990
(Babbini, 1991). (g) Faborso Bay (45° 7ʹ 9ʺ N, 13° 36ʹ 53ʺ E) near Rovinj during 1998–1999 (Zavodnik et al., 2002). (h) Rovinj area during 2003–2004 (Iveša, 2005). (i) Rovinj area during
the 1980s and 1997–1999 (Hanel, 2002). (j) Rovinj area in 2004 (Guidetti and Dulčić, 2007).
⁎ Observation of Cystoseira belts and forests without species identification.
166 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173
Fig. 2. Percent of the coastline occupied by Cystoseira amentacea (A) and sea urchin barrens (B) in the surveyed sectors scattered along the west Istria Coast during 2009–2013.
3.3. Eutrophication levels
Measurements of chlorophyll a (Fig. 4A, B) suggest that the eutro-
phication of the study area followed a decreasing trend throughout
the 1974–1988, 1989–1999 and 2000–2013 periods. This trend was ev-
ident at 0, 5 and 10 m in depth, but no differences were apparent at
Fig. 3. Chronology of the manifestation of the mucilage phenomenon in the northern
Adriatic Sea. Bold lines indicate the intense formation of voluminous mucilage
aggregates. Dashed lines indicate a weak manifestation of the mucilage phenomenon
(formation of aggregates showing a ribbon-like form).
20 m in depth and near the bottom (27 m). The same patterns were ob-
served during both the growth (March–August) and quiescence (Sep-
tember–February) phases of the Cystoseira vegetative cycle. Trends in
orthophosphate concentration were similar to those for chlorophyll a,
with slightly increased values near the bottom, during both the vegeta-
tive and quiescence Cystoseira phases (Fig. 4C, D), but the concentration
of nitrate during the 1989–1999 period (Fig. 4E, F) was lower than dur-
ing the 1974–1988 and 2000–2013 periods. Intermediate values were
obtained for the period 1974–1988, whereas the highest nitrate concen-
tration values were detected from 2000 to 2013. The patterns of nitrate
concentration in the water column during the Cystoseira species growth
and quiescence phases were similar (Fig. 4E, F), and the accumulation of
nitrate in the water column was likely caused by phosphorous limita-
tion due to a decrease in the phosphorous concentrations in the runoffs
of Italian rivers (Djakovac et al., 2012). However, the measured concen-
trations of nitrate were still within the range characteristic of oligotro-
phic Mediterranean waters (Vollenweider et al., 1992).
3.4. Visual assessment of C. amentacea and sea urchins
The visual surveys performed during the 2010–2013 period revealed
that C. amentacea was nearly exclusively present along the southern part
of the west Istrian Coast. Depending on the sector, C. amentacea covered
the upper level of the sublittoral zone (from the mean sea level to less
than 1 m in depth) of the rocky shore to varying degrees within a range
from 10 to 80% (Fig. 2A). Northward, we found well-developed patches
of C. amentacea around the two islands visited by Ercegović in 1950,
and at the St. Katarina Island station, patches of C. amentacea were
found at a depth of 1.5 m, i.e., below the upper level of the sublittoral
zone. According to Ercegović (1952), C. amentacea can dwell in depths
up to 3 m in the eastern Adriatic Sea, and in this study, C. amentacea
was only recorded below the upper level of the sublittoral at St. Katarina
Island.
During 2010–2013, sea urchin barrens have formed exclusively from
a depth of approximately 1 m to several metres, and the extent of the
barrens has generally increased along the coast from north (Cape
 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173 167

Fig. 4. Concentration of chlorophyll a (A and B), orthophosphate (C and D) and nitrate (E and F) from 1974 to 2013 at different depths at the RV001 oceanographic station from March–
August (A, C and E: Cystoseira vegetative phase) and September–February (B, D and F: Cystoseira quiescence phase) periods. Diamonds = 1974–1988; triangles = 1989–1999; and
circles = 2000–2013. Data are means ± SEM of measurements taken approximately monthly.

Savudrija) to south (Cape Kamenjak). In sectors of the northern and
central part of the peninsula that were surveyed, sea urchin barrens
were absent or their extent was very low, but in the south part of the
west Istria Coast, sea urchin barrens have been extending below the
zone that is intensely colonised by C. amentacea (Fig. 2B). Underwater
surveys using three randomly selected quadrats within each affected
sector showed that P. lividus formed the majority of the sea urchin bar-
rens. The density of P. lividus was 17.85 ± 2.34 individuals per m2
(mean ± SE; n = 36, i.e., 3 randomly placed quadrates × 12 sectors; bar-
rens were not present in the remaining 7 sectors: Fig. 2B). A. lixula was
found in small quantities only in sectors X, XIII and XIV, and its density
was 0.74 ± 0.29 individuals per m2 (mean ± SE; n = 9) in the barrens
of these sectors.
During the 2009 sampling of Cystoseira in the subtidal, sparsely dis-
tributed sea urchins were only observed in Cystoseira forests at shallow
depths (1–3 m) of stations R1, R2 and R3. During the 2010–2013 visual
surveys in the subtidal, small sea urchin barrens were observed in the
Rovinj area between 1 and 3 m in depth, but sea urchins were very
rare at greater depths. No relevant changes in the extent of Cystoseira
assemblages were observed.
3.5. Subtidal Cystoseira taxa
In the subtidal of each randomly selected station nested within the
three randomly selected areas, Cystoseira species formed continuous
forests, which suggests that the investigated habitat along the west
Istrian Coast was completely colonised by Cystoseira species. Depending
on the geomorphology of the coastline, this habitat extended from sev-
eral hundred metres to approximately 1 km along the coastline. All of
the expected Cystoseira species except C. amentacea were found at the
sampled depth ranges (0.5–2, 5–7 and 10–12 m). Cystoseira species
168 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173

Table 2
Biomass (g wet weight) of individual Cystoseira taxa and total Cystoseira biomass for samples collected along the west Istrian Coast at three depth ranges in spring 2009. Data are the means
and standard errors of nine 50 × 50 cm quadrates sampled within each of three stations, which were randomly selected within three areas of the west Istrian Coast (Novigrad, Vrsar and
Rovinj).

Taxa Novigrad 1 Novigrad 2 Novigrad 3 Vrsar 1 Vrsar 2 Vrsar 3 Rovinj 1 Rovinj 2 Rovinj 3

From 0.5 to 2 m in depth

C. barbata N.F. 530.9 ± 107.3 103.3 ± 58.5 169.0 ± 53.2 376.4 ± 78.8 77.0 ± 42.1 N.F. N.F. N.F.
C. c. compressa 53.6 ± 11.5 1.9 ± 1.1 14.6 ± 6.3 80.6 ± 44.9 216.2 ± 62.6 377.6 ± 87.0 244.2 ± 69.6 341.7 ± 84.6 8.2 ± 7.7
C. c. pustulata 164.6 ± 28.8 54 ± 50.3 53.0 ± 32.6 153.8 ± 50.3 131.7 ± 52.1 34.4 ± 34.4 N.F. 14.2 ± 6.4 N.F.
C. corniculata N.F. N.F. N.F. N.F. 1.0 ± 1.0 N.F. N.F. N.F. N.F.
C. crinita 41.0 ± 26.6 331.1 ± 77.9 281.3 ± 42.1 347.1 ± 58.4 134.7 ± 58.6 359.0 ± 61.7 180.4 ± 37.5 298.6 ± 82.4 249.0 ± 59.3
C. foeniculacea N.F. N.F. 1.2 ± 0.8 82.0 ± 32.2 19.4 ± 10.7 N.F. N.F. 46.9 ± 38.1 N.F.
C. spinosa N.F. N.F. N.F. N.F. N.F. N.F. N.F. N.F. N.F.
Total biomass 259.1 ± 24.7 918.1 ± 66.9 453.4 ± 56.2 832.4 ± 88.9 879.4 ± 88.3 848.0 ± 44.7 424.7 ± 51.7 701.3 ± 76.5 257.2 ± 66.0

From 5 to 7 m in depth
C. barbata 0.4 ± 0.3 33.9 ± 14.7 3.0 ± 2.5 105.2 ± 32.3 150.9 ± 47.3 30.1 ± 11.0 N.F. N.F. N.F.
C. c. compressa 3.7 ± 3.5 2.2 ± 1.4 8.3 ± 3.6 34.0 ± 16.5 79.6 ± 40.3 60.4 ± 15.0 272.2 ± 54.2 0.1 ± 0.1 N.F.
C. c. pustulata 56.2 ± 15.7 67.1 ± 12.7 46.1 ± 9.3 33.3 ± 12.2 167.9 ± 58.9 119.9 ± 22.7 3.0 ± 3.0 17.9 ± 11.6 5.4 ± 1.5
C. corniculata N.F. 328.6 ± 69.3 N.F. N.F. N.F. 12.8 ± 12.0 N.F. N.F. N.F.
C. crinita N.F. N.F. N.F. N.F. N.F. N.F. N.F. N.F. N.F.
C. foeniculacea 108.4 ± 34.8 11.1 ± 7.5 1.5 ± 1.5 4.1 ± 1.1 51.2 ± 12.4 33.9 ± 14.1 10.1 ± 5.6 152.0 ± 16.8 81.7 ± 12.2
C. spinosa N.F. 54.2 ± 16.9 23.2 ± 10.4 N.F. N.F. 16.2 ± 11.7 N.F. N.F. N.F.
Total biomass 168.8 ± 25.4 497.1 ± 61.5 82.2 ± 14.6 176.7 ± 24.5 449.5 ± 48.9 273.3 ± 26.5 285.3 ± 57.1 170.1 ± 24.7 87.1 ± 12.1

From 10 to 12 m in depth
C. barbata 5.0 ± 2.9 1.0 ± 1.0 0.4 ± 0.4 13.9 ± 3.5 10.1 ± 3.7 13.4 ± 12.1 N.F. 1.1 ± 0.7 1.3 ± 0.9
C. c. compressa 5.6 ± 3.1 N.F. 0.5 ± 0.4 2.5 ± 1.3 0.8 ± 0.6 4.0 ± 2.6 2.2 ± 0.6 N.F. 1.7 ± 1.7
C. c. pustulata 13.3 ± 3.7 N.F. 3.9 ± 1.5 2.0 ± 2.0 3.2 ± 1.5 0.4 ± 0.6 N.F. 0.2 ± 0.2 4.6 ± 1.4
C. corniculata 72.2 ± 38.3 643.8 ± 100.1 215.0 ± 55.6 15.1 ± 8.1 6.2 ± 2.2 255.4 ± 112.8 N.F. 73.3 ± 20.3 49.8 ± 14.6
C. crinita N.F. N.F. N.F. N.F. N.F. N.F. N.F. N.F. N.F.
C. foeniculacea 15.8 ± 5.1 1.2 ± 1.2 7.6 ± 3.4 30.9 ± 7.7 14.1 ± 3.5 2.2 ± 1.4 4.1 ± 2.2 6.6 ± 0.0 61.0 ± 9.0
C. spinosa 28.3 ± 21.8 109.6 ± 38.7 35.9 ± 11.6 N.F. N.F. N.F. N.F. 7.4 ± 5.0 15.2 ± 8.7
Total biomass 140.2 ± 41.1 755.6 ± 70.0 263.3 ± 54.2 64.4 ± 8.9 34.6 ± 6.9 275.6 ± 116.8 6.3 ± 1.9 88.7 ± 18.0 133.6 ± 13.0

Station locations are provided in Fig. 1; N.F. = not found.

formed mixed stands whose composition varied spatially and with
depth (Table 2).
PERMANOVA analyses (Table 3) detected a significant variation in the
composition of stands at the spatial scale of several kilometres, i.e., among
stations within sampling areas (P b 0.001 for all three depth ranges). Al-
though factor “Station” was random, we decided to conduct pairwise
comparison among stations within areas, and for the 0.5–2 m depth
range, all of the pair-wise tests were significant except for V1 versus V2
(P = 0.071) and R1 versus R2 (P = 0.285). For the 5–7 m depth range,
all of the pair-wise tests were significant except for those for the Vrsar
area (P N 0.05), and for the 10–12 m depth range, all of the pair-wise
tests were significant except for V1 versus V2 (P = 0.086). At the spatial
scale of tens of kilometres (among areas), a significant difference was
only detected for the depth range from 5 to 7 m (P = 0.046; Table 3).
However, the pair-wise tests did not have enough power to detect signif-
icant differences among areas. At the spatial scale of metres, i.e., among
the 50 × 50 cm quadrates within the 10 × 10 m plots, the level of patch-
iness was very high as indicated by the MS values of the residual at all of
the three depth ranges (estimates of the components of variation are pro-
vided in the Supplementary material).
For the depth range of 0.5 to 2 m, the most abundant species were
C. barbata, C. c. compressa and C. crinita, and C. foeniculacea and C. c.
pustulata showed intermediate biomass values (Table 2). Only one thal-
lus of C. corniculata was found (station V2), and C. amentacea and
C. spinosa were not found at this depth range. In general, both MDS
and cluster ordinations (Fig. 5A) revealed that the composition of
Cystoseira forests tended to be more similar among stations sampled
in different areas (spatial scale of tens of kilometres) than among
stations sampled in the same area (spatial scale of several kilometres).
Station N1 separated from all of the others due to high biomasses of
C. c. compressa and C. c. pustulata. Stations V2, N2 and V1 were
characterised by high C. barbata biomass, whereas stations N3 and R3
formed a cluster characterised by a high biomass of C. crinita. Both C. c.
compressa and C. crinita exhibited a high biomass values at stations R1,
V3 and R2 (Fig. 5A, Table 2).
For the depth range of 5 to 7 m, the most abundant taxa were
C. barbata, C. c. compressa, C. c. pustulata, C. corniculata, C. foeniculacea
and C. spinosa depending on the station (Table 2). MDS and cluster ordi-
nation (Fig. 5B) of stations showed the same general pattern as for the
0.5–2 m depth range; i.e., stations sampled in the same areas tended

Table 3
PERMANOVA analysing differences among the composition of Cystoseira forests at three depth ranges (A, B and C) in the subtidal of the west Istrian Coast.

A) 0.5–2 m in depth B) 5–7 m in depth C) 10–12 m in depth

Source DF SS MS Pseudo-F P SS MS Pseudo-F P SS MS Pseudo-F P

Area = A 2 31193 15597 1.4497 0.1898 61729 30865 1.8893 0.0457 39740 19870 1.3788 0.2181
Station(A) = S(A) 6 64550 10758 8.9632 0.0001 98017 16336 10.2000 0.0001 86465 14411 7.7134 0.0001
Plot(S(A)) 18 21605 1200 0.9716 0.5325 28829 1602 1.2075 0.1066 33629 1868 0.9731 0.5615
Residual 54 66707 1235 71623 2326 103670 1920

Factor “Area” is random with 3 levels (3 areas tens of kilometres distant from each other). Factor “Station” is random and nested in factor “Area” with 3 levels (3 stations several km distant
from each other within each area). Factor “Plot” is random and nested in factors “Area” and “Station” with 3 levels (3 plots tens of metres distant from each other within each station and
area). Number of replicates: n = 3, N = 81. Significant P values are in bold.
 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173 169

Fig. 5. Non-metric multidimensional scaling and cluster ordinations based on the Bray–Curtis dissimilarity measure for Cystoseira taxa sampled at 3 stations within the Novigrad (empty
quadrates), Vrsar (filled circles) and Rovinj (empty triangles) areas. A = from 0.5 to 2 m, B = from 5 to 7 m and C = from 10 to 12 m in depth. Superimposed influential taxa correspond to
a multiple correlation coefficient of 0.2.

to not cluster together. Station R1 formed a separate cluster because of a 4. Discussion

high biomass of C. c. compressa, and stations R3, N1 and R2 were
characterised by a high biomass of C. foeniculacea. Stations N2 and N3
formed separate clusters; C. c. pustulata and C. spinosa were abundant
at both stations whereas C. corniculata was only abundant at station
N2. At this depth, all stations in the Vrsar area formed a cluster due to
high C. barbata biomass (Fig. 5B, Table 2).
At the depth range of 10 to 12 m, the most abundant species were
C. corniculata, C. foeniculacea and C. spinosa, and C. barbata and C. c.
pustulata showed intermediate biomass values (Table 2). Additionally,
at this depth range, MDS and cluster ordinations indicated that the sim-
ilarity among stations tended to not be linked to the sampling areas
(Fig. 5C). Station R1 was characterised by a low abundance of Cystoseira
taxa, whereas C. corniculata and C. spinosa were very abundant at station
N2. Stations N3 and V3 formed a separate cluster because of a high
abundance of C. corniculata and C. c. pustulata, and a cluster composed
of stations V1 and V2 was characterised by a high abundance of
C. barbata. Cystoseira stands at stations R3, N1 and R2 were very similar
in composition; the most abundant species were C. corniculata,
C. foeniculacea and C. spinosa (Fig. 5C, Table 2).
We first aimed to evaluate the degree of recovery that Cystoseira
species attained along the west Istrian Coast during the period from
2009 to 2013. During the 1963–1968 period, Špan (1969) observed
that Cystoseira species formed rather abundant beds in the upper
infralittoral of the rocky mainland shore along the entire Croatian
Coast, but Špan (1969) did not provide quantitative data for the distri-
bution of individual Cystoseira species along the west Istrian Coast.
Munda (1972) reported sparse quantitative data on Cystoseira distribu-
tion for depths up to several metres before the regression phase that oc-
curred from the 1970s to the late 1990s. Therefore, the abundances of
Cystoseira species assessed for 2009–2013 were compared with those
from other Mediterranean areas where Cystoseira forests are considered
mature and not affected by anthropogenic pressure.
According to Ercegović (1952), only C. amentacea is able to dwell in
the upper sublittoral of the west Istrian Coast; in other Mediterranean
regions, Cystoseira mediterranea Sauvageau and Cystoseira tamariscifolia
(Hudson) Papenfuss are also able to colonise this zone (Thibaut et al.,
2014). During 2009–2013, C. amentacea was predominantly widespread
170 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173
along the south part of the Istrian Coast (Fig. 2A), showing cover values
similar to those reported for well-preserved stands in the northwestern
Mediterranean Sea (Mangialajo et al., 2008; Thibaut et al., 2014). In our
opinion, the rarity of C. amentacea along the north and central parts of
the Istrian Coast is likely not related to anthropogenic pressure, but
this situation could be produced by differences in wave action regimes.
As a rule, this alga colonises the upper sublittoral of coasts exposed to
wave action (Ercegović, 1952; Munda, 1979; Thibaut et al., 2014),
where it is likely to avoid desiccation during low tides. Due to the specif-
ic geographical orientation of the Istrian Peninsula, southern fetches are
longer than in the northern areas. The northeasterly Bora wind can be
very intense in the northern parts of the coast, but it blows from the in-
terior side of the peninsula to the coast and thus does not typically pro-
duce long fetches. However, intense Bora episodes can cause prolonged
periods of very low tides in these coastal areas during winter (Raicich,
2003, 2010), which could lead to exsiccation of the macroalgae
colonising the upper sublittoral zone (Martone et al., 2010).
At the depth range 0.5–2 m, C. barbata was particularly abundant in
the Novigrad and Vrsar areas (Table 2). This species prefers habitats that
are not exposed to wave action (Ercegović, 1952), so the absence of
C. amentacea in the upper sublittoral of these areas is plausible. The
other most abundant species at this depth range were C. crinita and
C. c. compressa, but to our knowledge, there are no studies depicting
mixed stands of C. barbata and C. crinita in the Mediterranean Sea in
the literature. C. barbata is considered rare in the Balearic Islands
(Sales and Ballesteros, 2009), and only sparse data are generally avail-
able for other Mediterranean regions (Ribera et al., 1992; Thibaut
et al., 2005; Mačić et al., 2010). It seems that C. barbata only forms ex-
tensive forests in the northern Adriatic Sea. In addition to the west
Istrian Coast, dense forests of C. barbata have also been described for
other northern Adriatic sites such as the Conero Coast in Italy
(Perkol-Finkel and Airoldi, 2010; Perkol-Finkel et al., 2012) and the
Slovenian Coast (Orlando-Bonaca et al., 2008). C. c. compressa
(Mangialajo et al., 2008; Mačić et al., 2010; Thibaut et al., 2015) and
C. crinita (Sales et al., 2012; Thibaut et al., 2015) are distributed through-
out the Mediterranean Sea.
The total mean Cystoseira biomass values assessed for the depth
range of 0.5 to 2 m in 9 randomly selected stations along the west Istrian
Coast ranged from approximately 1000 to 3600 g w.w. m−2 (estimated
from Table 2), but Munda (1972) reported higher total Cystoseira bio-
mass values of 4400 g w.w. m−2 for a station in the Rovinj area that
was sampled in April 1967. A biomass of 910 g d.w. m−2 was reported
for C. crinita assemblages at the same depth range in the northwestern
Mediterranean Sea (Bellan-Santini, 1968); assuming that the d.w. rep-
resents 20% of the w.w. of Cystoseira species (estimated from Munda,
1972), this value can be converted to 4550 g d.w. m−2. The fact that
lower values were obtained in this study might be due to the sampling
design; samples were collected randomly, whereas in other studies
samples were collected in patches showing maximum coverage values.
Thus, despite the higher biomass values estimated for the study area be-
fore the regression phase and for pristine northwestern Mediterranean
sites, we conclude that the Cystoseira assemblages inhabiting the 0.5–
2 m depth range recovered completely by 2009.
At the 5–7 m depth range, all of the expected Cystoseira species (ac-
cording to Ercegović, 1952) were found, i.e., C. barbata, C. c. compressa,
C. c. pustulata, C. corniculata, C. foeniculacea, and C. spinosa. All of these
species dominated at least one station, except C. spinosa which, howev-
er, was abundant at two stations (Table 2). To our knowledge, informa-
tion about the biomass of Cystoseira species for this depth range in the
Mediterranean Sea is scarce, but Munda (1993) mentioned that
C. foeniculacea forests were well developed in the subtidal of the Rovinj
area. However, the author did not provide quantitative estimates, and
C. foeniculacea is rare in pristine locations of the Balearic Archipelago
(Sales and Ballesteros, 2009) or locally extinct in some areas, such as
the Albere Coast (Thibaut et al., 2005) and the French Riviera (Nice–
Cannes–Monaco) (Thibaut et al., 2015). We suggest that natural local
processes, such as fish predation, bottom topography, current regime
and exposure to wave action, drove the observed variations in the com-
position of the Cystoseira forests colonising this depth range.
Recently, Sala et al. (2012) provided baseline data on the abundance
of canopy-forming macroalgae (i.e., Cystoseira species + Sargassum
vulgare C. Agardh) across the Mediterranean Sea (Spain, Italy, Greece
and Turkey) for the depth range of 8 to 12 m. According to these data,
after excluding 19 out of 32 of the stations sampled across the Mediter-
ranean Sea due to the very low biomass of canopy-forming macroalgae,
it can be estimated that the biomass varied from several hundred to ap-
proximately 2500 g w.w. m−2. The total mean Cystoseira biomass values
assessed in 2009 along the west Istrian Coast at the depth range of 10 to
12 m were low at only two stations (Table 2). For the remaining 7 sta-
tions, total mean biomass values ranged from approximately 250 to
3000 g w.w. m− 2 (estimated from Table 2), so we have no evidence
that recovered Cystoseira populations at the depth range of 10 to 12 m
along the west Istrian Coast have lower biomass than the most
flourishing canopy-forming assemblages at the same depths across
the Mediterranean Sea. The most abundant species at this depth range
were C. corniculata followed by C. foeniculacea and C. spinosa.
Nine Cystoseira taxa and S. vulgare have been reported as important
canopy-forming macroalgae across the Mediterranean at the depth
range from 8 to 12 m (Sala et al., 2012), but this study only found
S. vulgare in large quantities at station V3 (Vrsar area) at all of the sampled
depths. However, the wet weight of Sargassum was not taken into account
when calculating the total biomass at this station. Of the 9 Mediterranean
Cystoseira taxa, Cystoseira brachycarpa J. Agardh and Cystoseira elegans
Sauvageau were never reported for the northern Adriatic Sea; these spe-
cies are mostly abundant in the western basin of the Mediterranean Sea
(Gómez Garreta et al., 2001). The remaining 7 taxa reported for the Med-
iterranean Sea were: (1) C. barbata, (2) C. c. compressa, (3) C. c. pustulata
(4) C. corniculata, (5) C. foeniculacea f. latiramosa (Ercegović) A. Gómez
Garreta, M.C. Barceló, M.A. Ribera & J.R. Lluch (6) C. foeniculacea f.
tenuiramosa (Ercegović) A. Gómez Garreta, M.C. Barceló, M.A. Ribera & J.
Rull Lluch and (7) C. spinosa. Thus, even though only 8 of the approxi-
mately 40 Cystoseira taxa inhabiting the Mediterranean Sea have been re-
corded in the northern Adriatic Sea, the species characterising the
Cystoseira assemblages at depths of approximately 10 m are similar to
those for the Mediterranean Sea at the same depths.
A rapid recovery of C. barbata, C. c. compressa, C. c. pustulata and
C. foeniculacea might be expected because these species develop numer-
ous and voluminous aerocysts (Ercegović, 1952) that favour long-
distance dispersal. However, C. amentacea, C. corniculata, C. crinita and
C. spinosa, which produce smaller and less numerous aerocysts
(Ercegović, 1952), also showed a high recovery rate. This suggests that
these species never completely disappeared from the west Istrian Coast;
sparse patches likely persisted during the regression phase, forming the
base for the recovery during periods of favourable conditions.
Multidimensional analyses (Table 3, Fig. 5) revealed marked differ-
ences in the composition of mixed stands at the spatial scale of 2–
3 km (among stations within areas), but we eliminated anthropogenic
pressure as a driver of these patterns as all stations were located almost
3 km from urban areas. These differences could be produced by natural
factors acting at a local spatial scale, such as different levels of exposure
to wave action (Díez et al., 2003), the topographic heterogeneity of the
rocky bottom (Sales and Ballesteros, 2009; Navarro et al., 2011;
Devescovi, 2015) and the intensity of fish predation (Vergés et al.,
2014). Sea urchin predation was not a factor because the density of
sea urchins was very low in the subtidal of sampled areas (Fig. 2B).
Based on the above, Cystoseira assemblages recovered along the
west Istrian Coast after the regression that lasted from the 1970s to
the late 1990s, and their actual total abundance in the upper sublittoral
and subtidal zones can be considered to be similar to that in Mediterra-
nean sites with well-developed Cystoseira forests. In the northwestern
Mediterranean Sea, nitrate and orthophosphate can limit the growth
of C. mediterranea (Delgado et al., 1994), but nutrient limitation cannot
 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173
be assumed to be a cause of the decline in Cystoseira species in the
northern Adriatic because the regression period occurred when concen-
trations of nutrients in the water column were increasing. Local varia-
tions in the Cystoseira abundances assessed in 2009 also cannot be due
to nutrient limitation because, in general, the estimated Cystoseira
abundances were high. The long-term Cystoseira forest regression-
recovery phases (Table 1) have followed the eutrophication trends
assessed at the oceanographic station located in the Rovinj area
(Fig. 4), which reflects the overall variations in the eutrophication levels
of the northern Adriatic Sea (Djakovac et al., 2012; Giani et al., 2012).
The 1974–1988 period was characterised by high eutrophication levels,
and Cystoseira species nearly disappeared from the study area during
this time. Remnant patches of Cystoseira species persisted in rocky
pools and near some islands (Munda, 1982), likely forming the basis,
as producers of propagula, for the future recovery. During the 1989–
1999 period, eutrophication levels decreased to intermediate levels,
which mirrored the intensification of the mucilage phenomenon
(Fig. 3), and the first signs of Cystoseira species recovery were recorded
(Table 1). The 1985 ban on the use of polyphosphate in detergents and
the corresponding decrease in the concentration of orthophosphates in
Italian rivers (Degobbis et al., 2000; Cozzi and Giani, 2011) could have
promoted this decrease in eutrophication levels (Giani et al., 2012).
During the period 2000–2013, the northern Adriatic entered an
oligotrophication phase (Djakovac et al., 2012), and Cystoseira species
continued to recover along the west Istrian Coast (Table 1). In addition,
the formation of mucilage aggregates in the water column of the north-
ern Adriatic continued, but its intensity decreased after 2004 (Fig. 3).
The dynamics of mucilage events are generally thought to be generated
by a synergistic combination of several factors, of which the most im-
portant are the particular climatic and oceanographic conditions, nutri-
ent concentrations and nutrient ratios (Giani et al., 2005).
The long-term fluctuation in northern Adriatic eutrophication pat-
terns might directly and indirectly affect the Cystoseira regression-
recovery phases. Increased eutrophication can directly restrict macroalgal
growth through light limitation (Lavery et al., 1991; Valiela et al., 1997;
Menge et al., 2008; Kavanaugh et al., 2009), but eutrophication can also
indirectly affect the abundance of Cystoseira species by affecting the
abundance of sea urchins. In oligotrophic Mediterranean regions, the re-
cruitment of sea urchins positively correlates with planktonic primary
productivity (Cardona et al., 2013), so the oligotrophication of the north-
ern Adriatic Sea could have resulted in decreased sea urchin recruitment.
Finally, the mucilage aggregates may have indirectly promoted Cystoseira
recovery by negatively affecting sea urchin populations along the west
Istrian Coast through smothering and hypoxia. Deleterious effects of mu-
cilage aggregates on the macrozoobenthos of the northern Adriatic Sea
have been reported in several studies (Stachowitsch et al., 1990; Müller
et al., 1998), so it is possible that sea urchin populations were reduced
during periods of intense mucilage formation. However, profound delete-
rious effects of mucilage on Cystoseira species are less probable. Mucilage
aggregates can cause necrosis of deciduous branches, but the perennial
parts of Cystoseira thalli seem to be able to withstand the impact
(Devescovi and Iveša, 2007). Other effects, such as commercial sea urchin
harvest and fish predation, might also reduce sea urchin abundance, but
commercial harvesting along the west Istrian Coast started in 2014 after
the detected recovery of Cystoseira species. An increase in the abundance
of predatory fish resulted in the recovery of canopy-forming species in
the no-take reserve of Medes Islands (Spain) (Sala et al., 2012), but a sig-
nificant increase in sea urchin predators (mainly Sparidae; Guidetti and
Dulčić, 2007) is not expected along the west Istrian Coast, as it is one of
the most heavily fished areas of the Croatian Coast.
Acknowledgements
The authors would like to thank the individuals that contributed to
the collection of basic oceanographic data and the building of the CMR
datasets, particularly Dr. Robert Precali.
171
The study was supported by the European Community under the
INTERREG IIIA “Implementation of Water Quality Monitoring in the
Western Istria Coastal Sea — Northern Adriatic (WICOS)” Programme
and three projects from the Ministry of Science, Technology and Sport
of the Republic of Croatia (Project “Jadran”, Project 098-0982705-2731
and Project 098-0982705-2732).
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.marpolbul.2016.03.010.
References
Airoldi, L., Beck, M.W., 2007. Loss, status and trends for coastal marine habitats of Europe.
Oceanogr. Mar. Biol. 45, 345–405.
Asnaghi, V., Chiantore, M., Bertolotto, R.-M., Parravicini, V., Cattaneo-Vietti, R., Gaino, F.,
Moretto, P., Privitera, D., Mangialajo, L., 2009. Implementation of the European
water framework directive: natural variability associated with the CARLIT method
on the rocky shores of the Ligurian Sea (Italy). Mar. Ecol. 30 (4), 505–513.
Babbini, L., 1991. Evoluzioni delle fitocenosi infralitorali dell’alto Adriatico: Cystoseiretea.
Tesi in Algologia. Università degli studi di Trieste (124 pp.).
Ballesteros, E., 1988. Estructura y dinámica de la comunidad de Cystoseira mediterranea
Sauvageau en el Mediterráneo Noroccidental. Investig. Pesq. 52, 313–334.
Ballesteros, E., 1990. Structure and dynamics of the Cystoseira caespitosa Sauvageau
(Fucales, Phaeophyceae) community in the North-Western Mediterranean. Sci. Mar.
54, 155–168.
Ballesteros, E., Sala, E., Garrabou, J., Zabala, M., 1998. Community structure and frond size
distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the North-
western Mediterranean. Eur. J. Phycol. 33, 121–128.
Ballesteros, E., Torras, X., Pinedo, S., García, M., Mangialajo, L., De Torres, M., 2007. A new
methodology based on littoral community cartography dominated by macroalgae for
the implementation of the European water framework directive. Mar. Pollut. Bull. 55,
172–180.
Ballesteros, E., Garrabou, J., Hereu, B., Zabala, M., Cebrian, E., Sala, E., 2009. Deep-water
stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern
Mediterranean: insights into assemblage structure and population dynamics. Estuar.
Coast. Shelf Sci. 82, 477–484.
Bellan-Santini, D., 1968. Influence de la pollution sur les peuplements benthiques. Rev.
Int. Océanogr. Méd. 10, 27–53.
Bermejo, R., de la Fuente, G., Vergara, J.J., Hernández, I., 2013. Application of the CARLIT
index along a biogeographical gradient in the Alboran Sea (European Coast). Mar.
Pollut. Bull. 72 (1), 107–118.
Bianchi, C.N., 2007. Biodiversity issues for the forthcoming tropical Mediterranean Sea.
Hydrobiologia 580, 7–21.
Bianchi, C.N., Morri, C., 2000. Marine biodiversity of the Mediterranean Sea: situation,
problems and prospects for future research. Mar. Pollut. Bull. 40, 367–376.
Bianchi, C.N., Corsini-Foka, M., Morri, C., Zenetos, A., 2014. Thirty years after: dramatic
changes in the coastal marine ecosystems of Kos Island (Greece), 1981-2013.
Mediterr. Mar. Sci. 15, 482–497.
Cardona, L., Moranta, J., Reñones, O., Hereu, B., 2013. Pulses of phytoplanktonic productiv-
ity may enhance sea urchin abundance and induce state shifts in the Mediterranean
rocky reefs. Estuar. Coast. Shelf Sci. 133, 88–96.
Connell, S.D., Russell, B.D., Turner, D.J., Shepherd, S.A., Kildea, T., Miller, D., Airoldi, L.,
Cheshire, A., 2008. Recovering a lost baseline: missing kelp forests from a metropol-
itan coast. Mar. Ecol. Prog. Ser. 360, 63–72.
Cormaci, M., 1995. Struttura e periodismo dei popolamenti a Cystoseira (Fucophyceae,
Fucales) del Mediterraneo. G. Bot. Ital. 129, 357–366.
Cormaci, M., Furnari, G., 1999. Changes of the benthic algal flora of the Tremiti Islands
(southern Adriatic) Italy. Hydrobiologia 398 (399), 75–79.
Cormaci, M., Furnari, G., Catra, M., Alongi, G., Giaccone, G., 2012. Flora marina bentonica
del Mediterraneo: Phaeophyceae. Boll. Accad. Gioenia Sci. Nat. Catania 45, 1–508.
Cozzi, S., Giani, M., 2011. River water and nutrient discharges in the Northern Adriatic
Sea: current importance and long term changes. Cont. Shelf Res. 31, 1881–1893.
Degobbis, D., Fonda-Umani, S., Franco, P., Malej, A., Precali, R., Smodlaka, N., 1995. Chang-
es in the northern Adriatic ecosystem and the hypertrophic appearance of gelatinous
aggregates. Sci. Total Environ. 165, 43–58.
Degobbis, D., Malej, A., Fonda Umani, S., 1999. The mucilage phenomenon in the northern
Adriatic Sea. A critical review of the present scientific hypotheses. Ann. Ist. Super.
Sanità 35 (3), 373–381.
Degobbis, D., Precali, R., Ivančić, I., Smodlaka, N., Fuks, D., Kveder, S., 2000. Long-term
changes in the northern Adriatic ecosystem related to anthropogenic eutrophication.
Int. J. Environ. Pollut. 13, 495–533.
Delgado, O., Bellesteros, E., Vidal, M., 1994. Seasonal variation in tissue nitrogen and phos-
phorus of Cystoseira mediterranea Sauvageau (Fucales, Phaeophyceae) in the North-
western Mediterranean Sea. Bot. Mar. 37, 1–9.
Devescovi, M., 2015. Effects of bottom topography and anthropogenic pressure on north-
ern Adriatic Cystoseira spp. (Phaeophyceae, Fucales). Aquat. Bot. 121, 26–32.
Devescovi, M., Iveša, Lj., 2007. Short term impact of planktonic mucilage aggregates on
macrobenthos along the Istrian rocky coast (Northern Adriatic, Croatia). Mar. Pollut.
Bull. 54, 887–893.
172 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173
Díez, I., Santolaria, A., Gorostiaga, J.M., 2003. The relationship of environmental factors to
the structure and distribution of subtidal seaweed vegetation of the western Basque
coast (N Spain). Estuar. Coast. Shelf Sci. 56, 1041–1054.
Djakovac, T., Degobbis, D., Supić, N., Precali, R., 2012. Marked reduction of eutrophication
pressure in the northeastern Adriatic in the period 2000–2009. Estuar. Coast. Shelf
Sci. 115, 25–32.
Djakovac, T., Supić, N., Aubry, F.B., Degobbis, D., Giani, M., 2015. Mechanisms of hypoxia
frequency changes in the northern Adriatic Sea during the period 1972–2012.
J. Mar. Syst. 141, 179–189.
Draisma, S.G.A., Ballesteros, E., Rousseau, F., Thibaut, T., 2010. DNA sequence data demon-
strate the polyphyly of the genus Cystoseira and other Sargassaceae genera
(Phaeophyceae). J. Phycol. 46, 1329–1345.
EC, 2000. Directive 2000/60/EC of the European Parliament and the Council of 23 October
2000 Establishing a Framework for Community Action in the Field of Water Policy.
Legislative Acts and Other Instruments, ENV221 CODEC 513. European Union.
Ercegović, A., 1952. Jadranske cistozire. Njihova morfologija, ekologija i razvitak. – Sur les
Cystoseira adriatiques. Leur morphologie, ecologie et evolution. Fauna et Flora
Adriatica, IOR, Split (212 pp.).
Feldmann, J., 1937. Recherches sur la végétation marine de la Méditerranée. La Côte des
Albères. Rev. Algol. 10 (339 pp.).
Giaccone, G., Bruni, A., 1973. Le Cistoseire e la vegetazione sommersa del Mediterraneo.
Atti Ist. Veneto Sci., Lett. ed Arti Venezia 131, 59–103.
Giaccone, G., Alongi, G., Pizzuto, F., Cossu, A., 1994. La vegetazione marina bentonica
fotofila del Mediterraneo: II. Infralitorale e Circalitorale: Proposte di aggiornamento.
Boll. Accad. Gioenia Sci. Nat. Catania 27, 11–157.
Gianguzza, P., Agnetta, D., Bonaviri, C., Di Trapani, F., Visconti, G., Gianguzza, F., Riggio, S.,
2011. The rise of thermophilic sea urchins and the expansion of barren grounds in the
Mediterranean Sea. Chem. Ecol. 27, 129–134.
Giani, M., Rinaldi, A., Degobbis, D., 2005. Mucilages in the Adriatic and Tyrrhenian Sea: an
introduction. Sci. Total Environ. 353, 3–9.
Giani, M., Djakovac, T., Degobbis, D., Cozzi, S., Solidoro, C., Fonda Umani, S., 2012. Recent
changes in the marine ecosystems of the northern Adriatic Sea. Estuar. Coast. Shelf
Sci. 115, 1–13.
Gómez Garreta, A., Barceló Martí, M.C., Ribera Siguan, M.A., Rull LLuch, J., 2001. Cystoseira
C. Agardh. In: Gómez-Garreta, A. (Ed.), Flora Phycologica IbericaFucales vol. 1.
Universidad de Murcia, Murcia, pp. 99–166.
Guidetti, P., 2006. Marine reserve reestablish lost predatory interactions and cause com-
munity changes in rocky reefs. Ecol. Appl. 16, 963–976.
Guidetti, P., Dulčić, J., 2007. Relationships among predatory fish, sea urchins and barrens
in Mediterranean rocky reefs across a latitudinal gradient. Mar. Environ. Res. 63,
168–184.
Guidetti, P., Sala, E., 2007. Community-wide effects of marine reserves in the Mediterra-
nean Sea. Mar. Ecol. Prog. Ser. 335, 43–56.
Guidetti, P., Fraschetti, S., Terlizzi, A., Boero, F., 2003. Distribution patterns of sea urchins
and barrens in shallow Mediterranean rocky reefs impacted by the illegal fishery of
the rock-boring mollusc Lithophaga lithophaga. Mar. Biol. 143, 1135–1142.
Guiry, M.D., Guiry, G.M., 2015. AlgaeBase. World-wide Electronic Publication. National
University of Ireland, Galway (http://www.algaebase.org).
Hanel, R., 2002. Recovery of Fucacean association and associated fish assemblages in
the vicinity of Rovinj, Istrian coast, northern Adriatic Sea. Period. Biol. 104,
159–163.
Harley, C.D.G., Anderson, K.M., Demes, K.W., Jorve, J.P., Kordas, R.L., Coyle, T.A., Graham,
M.H., 2012. Effects of climate change on global seaweed communities. J. Phycol. 48,
1064–1078.
Hereu, B., 2006. Depletion of palatable algae by sea urchins and fishes in a Mediterranean
subtidal community. Mar. Ecol. Prog. Ser. 313, 95–103.
Iveša, Lj., 2005. Dinamika populacija makrofitobentosa na hridinastim dnima uz zapadnu
obalu Istre (Doktorska disertacija) Sveučilište u Zagrebu (160 pp.).
Jones, C.G., Lawton, J.H., Shachak, M., 1994. Organisms as ecosystem engineers. Oikos 69,
373–386.
Kang, C.-K., Choy, E.J., Son, Y., Lee, J.-Y., Kim, J.K., Kim, Y., Lee, K.-S., 2008. Food web struc-
ture of a restored macroalgal bed in the eastern Korean peninsula determined by C
and N stable isotope analyses. Mar. Biol. 153, 1181–1198.
Kavanaugh, M.T., Nielsen, K.J., Chan, F.T., Menge, B.A., Letelier, R.M., Goodrich, L.M., 2009.
Experimental assessment of the effects of shade on an intertidal kelp: do phytoplank-
ton blooms inhibit growth of open-coast macroalgae? Limnol. Oceanogr. 54,
276–288.
Lavery, P.S., Lukatelich, R.J., McComb, A.J., 1991. Changes in the biomass and species com-
position of macroalgae in a eutrophic estuary. Estuar. Coast. Shelf Sci. 33, 1–22.
Mačić, V., Antolić, B., Thibaut, T., Svircev, Z., 2010. Distibution of the most common Cystoseira
c. agardh species (Heterokontophyta, Fucales) on the coast of Montenegro (South-East
Adriatic Sea). Fresenius Environ. Bull. 19, 1191–1198.
Mangialajo, L., Chiantore, M., Cattaneo-Vietti, R., 2008. Loss of fucoid algae along a gradi-
ent of urbanisation, and structure of benthic assemblages. Mar. Ecol. Prog. Ser. 358,
63–74.
Martone, P.T., Alyono, M., Stites, S., 2010. Bleaching of an intertidal coralline alga:
untangling the effects of light, temperature, and desiccation. Mar. Ecol. Prog. Ser.
416, 57–67.
Menge, B.A., Chan, F., Lubchenco, J., 2008. Response of a rocky intertidal ecosystem engi-
neer and community dominant to climate change. Ecol. Lett. 11, 151–162.
Mineur, F., Arenas, F., Assis, J., Davies, A.J., Engelen, A.H., Fernandes, F., Malta, E.-J., Thibaut,
T., Van Nguyen, T., Vaz-Pinto, F., Vranken, S., Serrão, E.A., De Clerck, O., 2015.
European seaweeds under pressure: consequences for communities and ecosystem
functioning. J. Sea Res. 98, 91–108.
Molinier, R., 1960. Etude des biocénoses marines du Cap Corse. Vegetatio 9 (4–5),
217–312.
Müller, W.E.G., Riemer, S., Kurelec, B., Smodlaka, N., Puškarić, S., Jagić, B., Müller-Niklas, G.,
Queric, N.V., 1998. Chemosensitizers of the multixenobiotic resistance in amorphous
aggregates (marine snow): etiology of mass killing on the benthos in the Northern
Adriatic? Environ. Toxicol. Pharmacol. 6, 229–238.
Munda, I.M., 1972. The production of biomass in the settlements of benthic marine algae
in the northern Adriatic. Bot. Mar. 15, 218–244.
Munda, I.M., 1979. Some fucacean associations from the vicinity of Rovinj, Istrian Coast,
Northern Adriatic. Nova Hedwigia 31 (1–2), 607–666.
Munda, I.M., 1980a. Changes in the benthic algal associations of the vicinity of Rovinj
(Istrian coast, North Adriatic) caused by organic wastes. Acta Adriat. 21, 299–332.
Munda, I.M., 1980b. Survey of the algal biomass in the polluted area around Rovinj
(Istrian coast, North Adriatic). Acta Adriat. 21, 333–354.
Munda, I.M., 1982. The effects of organic pollution on the distribution of fucoid algae from
the Istrian coast (vicinity of Rovinj). Acta Adriat. 23, 329–337.
Munda, I.M., 1993. Changes and degradation of seaweed stands in the Northern Adriatic.
Hydrobiologia 260 (261), 239–253.
Munda, I.M., 2000. Long-term marine floristic changes around Rovinj (Istrian coast, North
Adriatic) estimated on the basis of historical data from Paul Kuckuck's field diaries
from the end of the 19th Century. Nova Hedwigia 71, 1–36.
Navarro, L., Ballesteros, E., Linares, C., Hereu, B., 2011. Spatial and temporal variability of
deep-water algal assemblages in the Northwestern Mediterranean: the effects of an
exceptional storm. Estuar. Coast. Shelf Sci. 95, 52–58.
Nikolić, V., Žuljević, A., Mangialajo, L., Antolić, B., Kušpilić, G., Ballesteros, E., 2013. Cartog-
raphy of littoral rocky-shore communities (CARLIT) as a tool for ecological quality as-
sessment of coastal waters in the Eastern Adriatic Sea. Ecol. Indic. 34, 87–93.
Orfanidis, S., Panayotidis, P., Stamatis, N., 2003. An insight to the ecological evaluation
index (EEI). Ecol. Indic. 3, 27–33.
Orlando-Bonaca, M., Lipej, L., Orfanidis, S., 2008. Benthic macrophytes as a tool for delin-
eating, monitoring and assessing ecological status: the case of Slovenian coastal wa-
ters. Mar. Pollut. Bull. 56, 666–676.
Perkol-Finkel, S., Airoldi, L., 2010. Loss and recovery potential of marine habitats: an ex-
perimental study of factors maintaining resilience in subtidal algal forests at the
Adriatic Sea. PLoS One 5 (5), e10791. http://dx.doi.org/10.1371/journal.pone.
0010791.
Perkol-Finkel, S., Ferrario, F., Nicotera, V., Airoldi, L., 2012. Conservation challenges in
urban seascapes: promoting the growth of threatened species on coastal infrastruc-
tures. J. Appl. Ecol. 49, 1457–1466.
Pinedo, S., Zabala, M., Ballesteros, E., 2013. Long-term changes in sublittoral macroalgal
assemblages related to water quality improvement. Bot. Mar. 56, 461–469.
Pinedo, S., Arévalo, R., Ballesteros, E., 2015. Seasonal dynamics of upper sublittoral assem-
blages on Mediterranean rocky shores along a eutrophication gradient. Estuar. Coast.
Shelf Sci. 161, 93–101.
Pitacco, V., Orlando-Bonaca, M., Mavrič, B., Popović, A., Lipej, L., 2014. Mollusc fauna asso-
ciated with the Cystoseira algal associations in the Gulf of Trieste (Northern Adriatic
Sea). Mediterr. Mar. Sci. 15 (2), 225–238.
Precali, R., Giani, M., Marini, M., Grilli, F., Ferrari, C.R., Pečar, O., Paschini, E., 2005. Mucilag-
inous aggregates in the northern Adriatic in the period 1999–2002: typology and dis-
tribution. Sci. Total Environ. 353, 10–23.
Raicich, F., 2003. Recent evolution of sea-level extremes at Trieste (Northern Adriatic).
Cont. Shelf Res. 23, 225–235.
Raicich, F., 2010. On the contributions of atmospheric pressure and wind to daily sea level
in the northern Adriatic Sea. Cont. Shelf Res. 30, 1575–1581.
Ribera, M.A., Gómez Garreta, A., Gallardo, T., Cormaci, M., Furnari, G., Giaccone, G., 1992.
Check-list of Mediterranean seaweeds. I. Fucophyceae (Warming, 1884). Bot. Mar.
35, 109–130.
Rodrìguez-Prieto, C., 1992. Estudi de l'estructura, la dinämica i la fenologia de la
comunitat de Cystoseira mediterranea Sauvageau: la importäncia de les minves
d'hivern. Mem. Doct. Ciènces, Inst. Ecol. aquat. Univ. autonoma Barcelona (187 pp.).
Sala, E., Boudouresque, C.F., Harmelin-Vivien, M., 1998. Fishing, trophic cascades, and the
structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82,
425–439.
Sala, E., Ballesteros, E., Dendrinos, P., Di Franco, A., Ferretti, F., et al., 2012. The structure of
Mediterranean rocky reef ecosystems across environmental and human gradients,
and conservation implications. PLoS One 7 (2), e32742. http://dx.doi.org/10.1371/
journal.pone.0032742.
Sales, M., Ballesteros, E., 2009. Shallow Cystoseira (Fucales: Ochrophyta) assemblages
thriving in sheltered areas from Menorca (NW Mediterranean): relationship with en-
vironmental factors and anthropogenic pressures. Estuar. Coast. Shelf Sci. 84,
476–482.
Sales, M., Cebrian, E., Tomas, F., Ballesteros, E., 2011. Pollution impacts and recovery po-
tential in three species of the genus Cystoseira (Fucales, Heterokontophyta). Estuar.
Coast. Shelf Sci. 92, 347–357.
Sales, M., Ballesteros, E., Anderson, M.J., Iveša, Lj., Cardona, E., 2012. Biogeographical pat-
terns of algal communities in the Mediterranean Sea: Cystoseira crinita-dominated as-
semblages as a case study. J. Biogeogr. 39, 140–152.
Sauvageau, C., 1912. A propos des Cystoseira de Banyuls et de Guéthary. Bull. Stat. Biol.
Arcachon 14 (424 pp.).
Seneš, J., 1989. North Adriatic inter-island shelf ecosystems of the Rovnj area. Geol.
Carpath. 40, 333–354.
Soltan, D., Verlaque, M., Boudouresque, C.F., Francour, P., 2001. Changes in macroalgal
communities in the vicinity of a Mediterranean sewage outfall after the setting up
of a treatment plant. Mar. Pollut. Bull. 42, 59–71.
Špan, A., 1969. Quantities of the most frequent Cystoseira species and their distribution in
the central and northern Adriatic. Proc 6th Int. Seaweeds Symp., pp. 383–387
Stachowitsch, M., Fanuko, N., Richter, M., 1990. Mucus aggregates in the Adriatic Sea: an
overview of stages and occurrences. PSZNI Mar. Ecol. 11, 327–350.
 L. Iveša et al. / Marine Pollution Bulletin 106 (2016) 162–173
Steneck, R.S., Graham, M.H., Bourque, B.J., Corbett, D., Erlandson, J.M., Estes, J.A., Tegner,
M.J., 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Envi-
ron. Conserv. 29, 436–459.
Strickland, J.D., Parsons, T.T., 1972. A practical handbook of seawater analysis. Bull. Fish.
Res. Board Can. 167 (310 pp.).
Thibaut, T., Pinedo, S., Torras, X., Ballesteros, E., 2005. Long-term decline of the popula-
tions of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France,
North-western Mediterranean). Mar. Pollut. Bull. 50, 1472–1489.
Thibaut, T., Blanfuné, A., Markovic, L., Verlaque, M., Boudouresque, C.F., Perret-
Boudouresque, M., Mačić, V., Bottin, L., 2014. Unexpected abundance and long-term
relative stability of the brown alga Cystoseira amentacea, hitherto regarded as a
threatened species, in the north-western Mediterranean Sea. Mar. Pollut. Bull. 89,
305–323.
Thibaut, T., Blanfuné, A., Boudouresque, C.F., Verlaque, M., 2015. Decline and local extinc-
tion of Fucales in the French Riviera: the harbinger of future extinctions? Mediterr.
Mar. Sci. 16, 206–224.
UNEP-PAM-RAC/SPA, 2012. Protocol concerning specially protected areas and biological
diversity in the Mediterranean. Annex II. List of Endangered or Threatened Species.
Paris, France, 8–10 February 2012 (7 pp.).
173
Valiela, I., McClelland, J., Hauxwell, J., Behr, P.J., Hersh, D., Foreman, K., 1997. Macroalgal
blooms in shallow estuaries: controls and ecophysiological and ecosystem conse-
quences. Limnol. Oceanogr. 42, 1105–1118.
Vergés, A., Alcoverro, T., Ballesteros, E., 2009. Role of fish herbivory in structuring the ver-
tical distribution of canopy algae Cystoseira spp. in the Mediterranean Sea. Mar. Ecol.
Prog. Ser. 375, 1–11.
Vergés, A., Tomas, F., Cebrian, E., Ballesteros, E., Kizilkaya, Z., Dendrinos, P., Karamanlidis,
A.A., Spiegel, D., Sala, E., 2014. Tropical rabbitfish and the deforestation of a warming
temperate sea. J. Ecol. 102, 1518–1527.
Verlaque, M., 1987. Contribution à l'étude du phytobenthos d'un écosystème photophile
thermophile marine en Méditerranée occidentale. Etude structurale et dynamique
du phytobenthos et analyses des relations Faune-Flore. Université d'Aix-Marseille II,
Marseille, France (PhD Thesis) (389 pp.).
Vollenweider, R.A., Marchetti, R., Viviani, R. (Eds.), 1992. Marine Coastal Eutrophication.
The Response of Marine Transitional Systems to Human Impact: Problems and Per-
spectives for Restoration. Elsevier, Amsterdam (1310 pp.).
Zavodnik, N., Iveša, Lj., Travizi, A., 2002. Note on recolonization by fucoid algae Cystoseira
spp. and Fucus virsoides in the North Adriatic Sea. Acta Adriat. 43, 25–32.