ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Original scientific article	DOI 10.19233/ASHN.2016.1
Received: 2016-03-16
DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC)
Claudio BATTELLI
Ulica Sergeja Masere 5, SI 6000 Koper, Slovenia e-mail: claudio_battelli@t-2.net
ABSTRACT
At the end of 2010, a significant decline in populations of Fucus virsoides was observed in the Slovenian coast (Gulf of Trieste, northern Adriatic), which prompted the undertaking of a direct observation assessment of changes in the occurrence of these populations along the Slovenian coast over the period 2010-2015. The paper presents a comparison between historical and current data on the presence of F. virsoides along the Slovenian coast, gathered through in situ surveys and from literature, and proposes the possible causes that have led to the decline and disappearance of F. virsoides populations along the Slovenian coastline.
Key words: Fucus virsoides, occurrence, disappearance, Slovenian coast, northern Adriatic
SCOMPARSA DI FUCUS VIRSOIDES J. AGARDH DALLA COSTA SLOVENA (GOLFO DI TRIESTE, ALTO ADRIATICO)
SINTESI
Un importante declino dei popolamenti a Fucus virsoides e stato osservato verso la fine del 2010 lungo la costa della Slovenia (Golfo di Trieste, Alto Adriatico). Nella nota vengono riportati i risultati di uno studio sulla distribuzio-ne di F. virsoides lungo la costa della Slovenia nelperiodo 2010-2015, attraverso !'osservazione diretta. Si mettono inoltre a confronto i dati storici con quelli attuali sulla presenza di F. virsoides in quest'area attraverso uno studio in situ e su fonti bibliografiche. Vengono avanzate delle ipotesi sulle possibili cause che hanno portato al rapido declino e alla successiva scomparsa di questa specie lungo la costa della Slovenia.
Parole chiave: Fucus virsoides, presenza, scomparsa, costa della Slovenia, Alto Adriatico
1
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
INTRODUCTION
The brown alga Fucus virsoides J. Agardh is the only species of the genus Fucus that occurs in the Adriatic Sea (Ardissone, 1886; Schiffner & Vatova, 1938; Linardic, 1949; Pignatti, 1962; Giaccone & Pignatti, 1967; Munda, 1972). In the past, it was the only brown alga and the most conspicuous canopy-forming macro-phyte to be found along the Slovenian coast, patchily distributed on the hard substrates of its midlittoral zone (Vukovič, 1980, 1982; Munda, 1993a; Battelli, 2002; Lipej et al., 2004; Rindi & Battelli, 2005; Battelli, 2013; Orlando-Bonaca et al. 2013). F. virsoides has been recorded along the Adriatic shores from Venice in Italy to Albania (e.g., Linardic, 1949; Kashta, 1995/96; Mačic, 2006). It is not clear which factors limit its occurrence. In addition to geomorphological characteristics, the key limiting factors are probably high salinity and high average annual temperatures (Vouk, 1938; Linardic, 1949). In recent years, particular attention has been paid to climate-related variables (Boero & Bonsdorff, 2007; Boero et al. 2008; Munda, 2008).
In studies carried out to date, the distribution pattern and abundance of F. virsoides have been related to substratum configuration, exposure to winds, wave direction (Lipizer et al., 1995; Orlando-Bonaca et al., 2013), low salinity of sea water (Vouk, 1938; Linardic, 1949; Giaccone & Pignatti, 1967; Munda, 1972), low concentration of pollutants (Vukovič, 1980, 1982; Munda & Kremer, 1977; Kremer & Munda, 1982; Munda, 1972, 1981, 1982, 1991, 1993a, 1993b), and type of substratum (Vukovič, 1982; Battelli, 2002; Rindi & Battelli, 2005; Battelli, 2013). Several authors revealed the midlittoral zone to be an extremely variable environment, characterized by periodic fluctuations of several ecophysiological parameters during the tidal cycles, such as light, temperature, hydrodynamics and grazing (Pignatti, 1962; Giaccone & Pignatti, 1967; Munda, 1972; Battelli, 2013).
The impact of anthropogenic disturbance on the structure, dynamics and composition of the macroalgal midlittoral assemblages of northern Adriatic was highlighted by several authors (Lipizer et al., 1995; Vukovič, 1980, 1982; Munda, 1993a, 1993b, 2000; Battelli, 2002; Rindi & Battelli, 2005; Lipej et al., 2004, 2006; Falace et al., 2010; Orlando-Bonaca et al., 2013).
The use of historical data in marine ecology provides a valid instrument for detecting and understanding recent changes that may occur in marine ecosystems particularly due to human activities (Jackson et al., 2001). This approach is also important for designing appropriate policies for habitat management and conservation, so that the changes can be assessed through long-term analysis (e.g. Falace et al., 2010).
A significant decline in the abundance of populations of this species was observed at the end of autumn 2010 along the entire Slovenian coast (Gulf of Trieste, northern Adriatic). This appears to be the largest decline
event ever recorded in the midlittoral assemblages of this area. To date, no explanation has been proposed about the cause(s) of this event.
In order to illustrate the decline of F. virsoides populations along the Slovenian coast, their historical distribution was compared to recent field observations. The aims of this study were: (a) to summarize the distribution of F. virsoides along the Slovenian coast based on literature information, and (b) to document the state of the populations of the species in this area during the period 2010-2015. Based on the current distribution, the possible causes of and the factors responsible for the observed disappearance of F. virsoides populations are proposed.
MATERIAL AND METHODS Study area
The Slovenian coast is located in the southern part of the Gulf of Trieste and extends for approximately 46 km from Sv. Jernej's Bay (the cape Debeli rtic - the north side of the Koper Bay) to the Dragonja River (Piran Bay - near the Croatian border). Most of the shore is influenced by dominant winds blowing from North-NorthEast and from South-East. The sea surface temperature generally ranges between a minimum of 7 °C in February and a maximum of 28 °C in August; the salinity from 28 in spring and summer to 36-37 in winter. The vertical extent of the midlittoral zone (between Mean Higher High Water and Mean Lower Low Water) is approximately 90 cm (ARSO, 2015). The Slovenian coastal area is characterized by its two main bays: Koper Bay and Piran Bay. The rocky substrate consists mainly of Eocene flysch layers, with alternating solid sandstone and soft marl (Ogorelec et al., 1997); in the area of Izola (San Simon), the coast is formed of Alveoline-nummu-litic limestone (Pavlovec, 1985). The morphology of the coastline varies from steep flysch cliffs to sloping beaches mainly composed of allochthonous substrata made of sandstone and marl gravel, and pebbles of different size. In the recent decades, the Slovenian coastal area has been subjected to many anthropogenic influences such as farming, mariculture, urbanization and large-scale tourism-related activities, with the result that nowadays only about 18% of the shore can be considered in its natural state (Turk et al., 2007).
Historical information about the presence of Fucus virsoides
Long-term changes of the F. virsoides populations along the Slovenian coast were analysed and a comparison was made between historical data on the occurrence of these communities in the past and in the period 2010-2015. Only the collectors who gathered samples of F. virsoides from the Slovenian coast were cited. The first record dates back to 1856 - Pius Titius (1801-1884)
2
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
collected the species along the coast of Piran under the name Fucus sherardi (specimens held in the Herbarium of the Slovenian Museum of Natural History, Ljubljana) (Alberti & Battelli, 2002). Giuseppe Accurti (18241907), in 1858, first mentioned the presence of this alga along the shores of Koper Bay. In 1858, he published the article "Cenno sulle alghe di Capodistria", in which he described in detail 195 species of algae collected in Koper Bay. Another important collector of marine organisms of this period was Antonio Zaratin (1846-1923). His herbarium contains nine samples of F. virsoides: two of them, collected in Koper Bay (one in September 1886 and the other in March 1910) and reported as F. vesicu-losus Ag., are part of, respectively, the "Herbarium Pata-vinum" collection of the Botanical Museum of Padua, and the "Flora marina Iustinopolitana" collection of the Gian Rinaldo Carli Gymnasium, Koper. Five samples of F. virsoides were collected in Koper Bay as F. Scherardi Ag. in May 1886, September 1886, October 1909, January 1910 and May 1910, and they are all preserved in the above-mentioned "Flora marina Iustinopolitana". The oldest voucher samples of the Zaratin collection were collected in Piran Bay in August 1885 as F. Sherardi Ag., and are currently conserved at the Ruder Boskovic Institute Centar za istrazivanje mora, Rovinj - Centre for Marine Research, Rovinj (Croatia) (Battelli & Alberti, 2003).
Historical information about the distribution
of F. virsoides populations
The past distribution of F. virsoides on the Slovenian coast was assessed using data obtained from a variety of sources, including all available published literature dealing with the presence of F. virsoides on the Slovenian coast (Accurti, 1858; Stirn, 1965; Matjasic & Stirn, 1975; Chiesa & Lorenzoni, 1980; Vukovic, 1980, 1982; Munda, 1991, 1993a, 1993b; Battelli, 1999, 2002; Alberti & Battelli, 2002; Battelli & Alberti, 2003; Lipej et al., 2004; Orlando-Bonaca et al., 2013).
The first map of the distribution of F. virsoides along the Slovenian coast was drawn by Stirn (1965). Among subsequent publications, some presented detailed maps of the area in its totality (Lipej et al., 2004; Orlando-Bonaca et al., 2013), others only in parts (Piran Bay by Vukovic, 1980, and Koper Bay by Vukovic, 1982).
Environmental parameters
Data of several physical and chemical parameters of the sea surface, provided by the Environment Agency of the Republic of Slovenia (ARSO), were analysed. The selected parameters included: temperature (°C), salinity, nitrites (|jmol NO2/l), nitrates (|jmol NO3/l), ammonia (|jmol NH4), orthophosphates (jmol PO4/l), total nitrogen (jmol N/l) and silicate (jimol SiO2/l). The monthly means of these data were grouped into seasonal means for the period 2005-2014. The latter period was divid-
ed into two main periods, 2005-2010 and 2011-2014, since the onset of the decline of F. virsoides populations was observed in late 2010.
Field work: observations in the period 2010-2015
The distribution of F. virsoides on the Slovenian coast in the years 2010-2015 was assessed through year-round field observation, grouping the data by season (i.e. winter comprised the data for January, February and March; spring comprised the data for April, May and June; summer comprised the data for July, August and September; autumn comprised the data for October, November and December). We inspected the whole Slovenian coastline at selected sites, as shown in Table 1, from Sv. Jernej's Bay (the cape Debeli rtič) to the Dragonja River (near the Croatian border), paying special attention to the sites sampled by previous researchers.
The occurrence of F. virsoides was assessed visually along the coast during low tide, as the latter provides the best conditions for direct observations. For this purpose, the semi-quantitative categories for the abundance of macroalgae, based on the work of Ballesteros et al. (2007) and tested by Orlando-Bonaca et al., (2013), were used: F1= rare to scattered thalli, F2 = abundant patches, F3 = a continuous or almost continuous belt.
The vertical extent of the midlittoral surveyed zone was approximately 1 m and included sandstone and limestone boulders that are not moved by most waves, breakwaters composed of limestone, and sandstone boulders. Excluded from the survey were river mouths, inner parts of commercial harbours, sites to which access was forbidden (such as marinas, hotel beaches, etc.), areas composed of marl, and mobile substrates such as sand, mud, or pebbles, which are mobile in wave conditions, as they are all unsuitable for the development of F. virsoides.
Sampling of Patella caerulea
During the period 2010-2015, an increase in the number of the main grazers of the midlittoral zone, P caerulea, was observed (pers. obs.). Therefore, throughout April 2015, the density of P. caerulea in the rocky midlittoral zone was assessed in 20 sites distributed along the Slovenian coast (from Sv. Jernej's Bay - the cape Debeli rtič to the Sečovlje saltpans). The study examined the same sites as the previous researchers who studied the occurrence of F. virsoides populations. In order to estimate the density of P. caerulea, the individuals were counted in five randomly chosen 400 cm2 (20 x 20 cm) quadrats at each selected site.
Data analyses
To evaluate the differences between seasonal mean values of physical and chemical parameters of the sea
3
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
□ % % M	tA 46 40
	d 9
	- S 15 ^ KOPER ^Jj IZOLA W PIRAN
A ° A g	19,.;.' 4S"Jb JJ
Fig. 1: Maps of the distribution of Fucus virsoides according to historical and recent data: (A) Štirn (1965); (B) Vu-kovič (1982); (C) Lipej et al. (2004); (D) Orlando-Bonaca et al. (2013); (E) this study, before autumn 2010, and (F) this study, during the period 2011-2015. The black bold lines with numbers indicate the presence of F. virsoides. Sl. 1: Zemljevid razširjenosti vrste Fucus virsoides glede na zgodovinske in novejše podatke: (A) Štirn (1965); (B) Vukovič (1982); (C) Lipej et al. (2004); (D) Orlando-Bonaca et al. (2013); (E) pričujoče delo; pred jesenjo 2010 in (F) pričujoče delo; v obdobju 2011-2015. Črne črte s številkami označujejo pojavljanje vrste F. virsoides.
4
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
surface, the non-parametric Kruskal-Wallis test was used.
RESULTS AND DISCUSSION
Long-term distribution of F. virsoides populations
The historical and current distribution of the populations of F. virsoides along the Slovenian coastline is illustrated in Figure 1. Comparisons between the single distribution reports by Stirn (1965), Vukovic (1982), Lipej et al. (2004), Orlando-Bonaca et al. (2013) and the present study, for the period before autumn 2010, show an increase in the distribution of this species all along the Slovenian coast. To date, no explanation about the cause(s) of this event has been proposed.
A comparison between the distribution of F. virsoides before autumn 2010 (Fig. 1A, 1B, 1C, 1D, 1E) and the findings of the present study covering the period 20112015 (Fig. 1F) reveal a drastic decline that began after autumn 2010.
In the period from the winter to summer 2010, F. virsoides was present along the Slovenian coastline from Sv. Jernej's Bay (Debeli rtič - near Italian border) to the Sečovlje saltpans (near the Croatian border) (Fig. 1E) with an abundance that ranged between rare to scattered thalli (F1) and a continuous or almost continuous belt (F3) according to the substrates favourable for the development of this species. In Koper Bay, F. virsoides was sparsely distributed from Debeli rtič to Sv. Katarina's Bay, Ankaran (sites 1-5), with an abundance of rare to scattered (F1) because of the presence
No site	Site	Period					
		2010 (W, Sp, Su)	2010 A	2011 (W, Sp, Su, A)	2013 (W, Sp, Su, A)	2014 (W, Sp, Su, A)	2015 (W, Sp, Su, A)
1	Sv. Jernej Bay	F1	-	-	-	-	-
2	Cape Debeli rtič	F1	-	-	-	-	-
3	Port - Cape Debeli rtič	F1	-	-	-	-	-
4	Valdoltra	F1	-	-	-	-	-
5	Sv. Katarina	F1	-	-	-	-	-
6	Porporela harbor, Koper	F2	-	-	-	-	-
7	Koper - Semedela	F2	-	-	-	-	-
8	Koper - Izola	F2	-	-	-	-	-
9	Viližan bay	F2	F1	F1	F1	-	-
10	Izola	F3	-	-	-	-	-
11	San. Simon	F3	-	-	-	-	-
12	Cape Kane Strunjan	F1	-	-	-	-	-
13	Cape Strunjan	F1	-	-	-	-	-
14	Strunjan saltpans	F1	-	-	-	-	-
15	Fiesa-Madona - Piran	F1	-	-	-	-	-
16	Cape Madona Piran	F2	-	-	-	-	-
17	Bernardin	F1	-	-	-	-	-
18	»Pirat« Bernardin	F1	F1	F1	F1	F1	-
18a	Fizine	F1	-	-	-	-	-
19	Cape Seča	F1	-	-	-	-	-
20	Sečovlje saltpans	F1	-	-	-	-	-
5
Tab. 1: Occurrence and abundance (semi-quantitative) of Fucus virsoides in investigated sites, during different seasons. Legend: Sp - spring, Su - summer, A - autumn, W - winter, F1=rare to scattered thalli; F2=abundant patches; F3=a continuous or almost continuous belt.
Tab. 1: Prikaz raziskanih mest pojavljanja bračiča (Fucus virsoides) in njegove abundance (semi-kvantitativne), v različnih časovnih obdobjih. Legenda: Sp - pomlad, Su- poletje, A- jesen, W - zima, F1=redke do razpršene steljke; F2=gručasta razporeditev; F3=skoraj sklenjen do sklenjen pas.
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
of mobile substrata composed mainly of sand or marl and sandstone mobile pebbles in wave conditions. In the southern part of Koper Bay (along the coast between Koper and Izola in sites 7-9), F. virsoides populations were dominant on breakwaters with an abundance ranging from scattered thalli (F1) to abundant patches (F2). In the vicinity of ports and main urban areas (Koper, Izola and Piran; sites 6, 10, 16), where the coast is completely artificialized, only a few patches were preserved (F2). In the inner parts of the ports, F. virsoides was present as isolated individuals (F1) or in small patches (F2). The largest populations in abundant patches (F2) and in a continuous or almost continuous belt (F3) were observed on the limestone rocky coast all around Izola and Korbat Cape in San Simon near Izola (sites 10 and 11). Along the natural coast (sites 12, 13, 14, 15) extending from San Simon to the Cape of Strunjan, populations of F. virsoides were more fragmented with an abundance ranging from rare to scattered (F1) due to the presence of substrata unsuitable for the development of this alga, i.e. substrata composed mainly of sand, mud or marl and of sandstone pebbles that are mobile in wave conditions. A similar situation was observed on the coast stretching from Piran to Forma viva (sites 17-19), near Lucija, and on the breakwaters along the external part of the Secovlje saltpans (site 20).
Decline of Fucus virsoides populations
During the period from autumn 2010 to autumn 2015, the situation of F. virsoides populations turned critical. One of the most striking observations was that no attached F. virsoides and not even one individual thal-lus was observed during field observation in this period, except for sites 9 and 18. At Vilizan Bay (site 9), near Izola, and in the inner part of the Sailing Club Pirat near Bernardin (Piran Bay, site 18) (Fig. 1F; Tab. 1), F. virsoides were scattered or present with only rare thalli (F1).
Up to 2013, a few small individuals (F1) were observed growing on small natural sandstone pebbles at Vilizan Bay, while at Bernardin a very small, patchily distributed population (F2) was observed on an artificial concrete surface of about 6 m2, but unfortunately only up until autumn 2014 (Tab. 1).
Environmental parameters
From the comparisons of sea surface chemical parameters for the Slovenian coastal sea (MOP, ARSO, 2015), shown in Figure 2, it is evident that the differences in the mean values of single chemical parameters during the periods 2005-2010 (before the decline of F. virsoides populations) and 2011-2014, barring a few exceptions, are not that remarkable.
For instance, compared to the period 2005-2010, before the decline of the F. virsoides populations, the
concentrations of nitrates in the period 2011-2014 were in general slightly lower in all seasons, but the difference was statistically non-significant. A very similar situation was found for total nitrogen, while in silicates, during the summer period, the differences in concentration were statistically significant (P < 0.001). For nitrites the concentration was higher—but not statistically significant—in winter and summer during the period 2011-2014. An increase in the concentration of orthophosphate was observed for almost all seasons in the period 2011-2014, especially in spring, when the difference was statistically significant (P < 0.01), and autumn, whereas in summer a slight but statistically non-significant decrease would occur. The concentration of ammonia was higher in winter, spring and summer in the period 2011-2014, but with statistical significance only in spring (P < 0.05) and summer (P < 0.01). The salinity was higher in all seasons except for summer, but not statistically significant. We noticed that the trend and the values of sea temperature remained very similar and statistically non-significant in all seasons in both periods (Fig. 2).
Two decades ago it was found that the trophic conditions in the Gulf of Trieste do not exert a significant impact on the distribution of F. virsoides (Lipizer et al., 1995). During our observation many populations of F. virsoides were found growing inside small harbours or along boatyards, where fluctuations in salinity and nutrient concentrations are frequent, which is consistent with Lipizer et al. (1995) and Orlando-Bonaca et al. (2013). Although F. virsoides is able to tolerate a wide range of salinity and temperature, our opinion is that it is necessary to confirm this with experimental data, because at the present we do not know the limits of survival of this species in relation to salinity and temperature. According to several authors (e.g., Vouk, 1938; Linardic, 1949; Giaccone & Pignatti, 1967; Munda, 1972; Mačic, 2006), the limiting factors for the presence of F. virsoides seem to be extreme salinity and temperatures.
F. virsoides is considered an alga with a great tolerance to high pollution levels and variation in many environmental factors such as temperature, salinity, wave exposure, etc. (Lipizer et al., 1995; Orlando-Bonaca et al., 2013). At present we do not know what factor(s) should be considered the potential reason(s) for this drastic event.
The presence and abundance of grazers
During autumn 2010 (when the first decline of F. virsoides was noticed) a substantial increase in the individuals of P. caerulea distributed among and immediately above the F. virsoides populations was observed, but not evaluated.
The hypothesized increased densities of grazers can lead to the loss of dominant habitat forming species, such as F. virsoides. The main grazer that is involved in
6
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
limo I
7,00 6,00 5,00 4,00 3,00 2,00 1,00 0,00
Si02/L
II I I
summer	autumn
nmol P04/L
0,12
0,1 0,08 0,06 0,04 0,02 0
M
summer	autumn
Salinity
37,50 37,00 36,50 36,00 35,50 35,00 34,50 34,00 33,50
llll
spring	summer
T/°C
30,00 25,00 20,00 15,00 10,00 5,00 0,00
■ I I I
spring summer autumn
Fig. 2: Seasonal values (mean ± SE) of sea surface chemical parameters (silicate, nitrogen, orthophosphate, nitrate, nitrite, ammonia and salinity) and physical parameters (temperature) during the periods 2005-2010 (black columns) and 2011-2014 (grey columns) for the Slovenian coastal sea (Source of data: MOP, ARSO, 2015 - http:// www.arso.gov. si/en/).
Sl. 2: Sezonske vrednosti (povprečje ± SN) kemijskih (silikati, dušik, ortofosfati, nitrati, nitriti, amonijak in slanost) in fizikalnih (temperatura) parametrov v obdobjih 2005-2010 (črni stolpci) in 2011-2014 (sivi stolpci) v površinskem sloju slovenskega morja (Vir podatkov: MOP, ARSO, 2015 - http://www.arso.gov.si/en/).
7
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
this process along the Slovenian coast is P. caerulea (De Min & Vio, 1997). Population densities of this species in different study sites are shown in Table 2. The densities occurring at the sites situated along the coastline between Koper and Izola and at Bernardin (both 11/400 cm2) were higher than the average of limpets at selected sites along the Slovenian coastline. The minimum density was observed at site KP Semedela (3/400 cm2).
The massive presence of P. caerulea along the Slovenian coastline leads us to consider the possibility that this might be one of the factors explaining the decline of F. virsoides populations. Our field observations are supported by several previous studies that considered limpets, such as P. caerulea, as important structuring agents
of midlittoral communities, controlling the distribution of algae (Arrontes et al., 2004). It is well documented that the composition and dynamics of midlittoral communities in rocky shores are strongly influenced by the activity of grazers (Hawkins et al., 1992; Jenkins et al., 1999; Arrontes et al., 2004). It is obvious that not all species in the grazer assemblage have the same effect on algae (Underwood & Jernakoff, 1981). Other gastropods (Cervin & Aberg, 1997, Viejo et al., 1999), chitons (Dethier & Duggins, 1984) or crustaceans may play relevant roles, but limpets are very often the key grazers in midlittoral zone (Hawkins et al., 1992; Johnson et al., 1997, 1998; Jonsson et al., 2006).
CONCLUSIONS
There are probably several reasons for the observed decline of F. virsoides populations. Many factors have been suggested as possible causes of this occurrence, including urbanization and eutrophication (Gessner, 1969; Gessner & Hammer, 1971; Munda, 1981, 1982; Kremer & Munda, 1982, Vukovic, 1982; Munda, 1993a, 1993b; Munda & Veber, 1996), as well as climate change (Munda, 2008). Some authors (e.g., Munda, 1981; Kremer & Munda, 1982; Vukovic, 1982; Munda, 1997) suspect that an excess of nitrates may be responsible for the disappearance of F. virsoides populations from polluted sites, although Lipizer et al. (1995) considers F. virsoides to have a great tolerance to high pollution levels. The comparison of seasonal variation of nitrates during the period before the disappearance of this species with the values after its decline indicates a slight decrease in these values. Therefore, we are inclined to consider this parameter as insufficient to trigger this event. Describing the benthic vegetation in the midlittoral zone of Koper Bay, Vukovic (1982) highlights the presence of F. virsoides populations on solid substrates (natural sandstone and jetties) along the entire coastline from the cape Debeli rtic to Izola with preference for limestone, which is in accordance with our observations.
Based on our 2010-2015 field observations, the F. virsoides populations along the Slovenian coast can be considered highly endangered, and the high density of limpets, present all along the Slovenian coast, might be one of the factors explaining the decline of F. virsoides populations and, consequently, their disappearance.
More environmental data is needed to be able to establish precisely the causes leading to the decline of F. virsoides populations in the Slovenian coast. Experimental data is also needed on the effects of organic and chemical pollution on this species. The role of grazers, such as P. caerulea, highlighted in this study, deserves further attention, too. Therefore, we strongly believe that further research and monitoring programmes of biological, physical and chemical parameters are necessary to evaluate the level of their impact on F. virsoides populations.
Tab 2. Average density (number of specimens/400 cm2) of Patella caerulea at selected sites along the Slovenian coast during April 2015.
Tab. 2: Povprečna gostota (št. osebkov/400 cm2) vrste Patella caerulea na izbranih postajah vzdolž slovenske obale v aprilu 2015.
No site	Site	Density (individuals/ 400 cm2)	stdev
1	Sv. Jernej's Bay	5.00	0.71
2	Cape Debeli rtič	5.20	0.84
3	Port - Cape Debeli rtič	8.80	3.35
4	Valdoltra	5.25	0.45
5	Sv. Katarina's Bay	5.00	1.00
6	Porporela harbor, Koper	8.80	4.15
7	Koper - Semedela	3.00	0.71
8	Koper - Izola	11.00	3.65
9	Viližan Bay	5.80	0.84
10	Izola	4.80	0.45
11	San Simon	7.40	2.30
12	Cape Kane Strunjan	9.40	3.05
13	Cape Strunjan	7.60	1.14
14	Strunjan saltpans	5.80	2.49
15	Fiesa-Madona - Piran	7.80	2.17
16	Cape Madona Piran	7.40	2.30
17	Bernardin	11.00	6.08
18	»Pirat« Bernardin	4.80	1.30
18a	Fizine	8.50	1.92
19	Cape Seča	8.00	2.51
20	Sečovlje saltpans	3.60	1.14
	Total of averages	5.96	2.99
8
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
ACKNOWLEDGEMENTS
We are grateful to Valter Ziza from the Aquarium of Piran and Marjan Richter, for their important information on the distribution of Fucus virsoides along the Slo-
venian coast. Special thanks to Mateja Poje, MSc, from the Slovenian Environment Agency - Ministry of the Environment and Spatial Planning for providing all physical and chemical data of Slovenian sea surface.
9
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
IZGINOTJE BRAČIČA (FUCUS VIRSOIDES J. Agardh) IZ OBALE SLOVENIJE (TRŽAŠKI ZALIV, SEVERNI JADRAN)
Claudio BATTELLI
Ulica Sergeja Mašere 5, SI 6000 Koper, Slovenia e-mail: claudio_battelli@t-2.net
POVZETEK
V članku avtor poroča o izrazitem upadanju bračiča (Fucus virsoides) vzdolž obale Slovenije (Tržaški zaliv, severni Jadran), ki se je začelo proti koncu leta 2010. Podaja rezultate o razširjenosti bračiča v Sloveniji v obdobju 2010-2015, ki jih je avtor pridobil na podlagi opazovanja na terenu (in situ). Avtor primerja zgodovinske podatke o pojavljanju bračiča na tem območju s sedanjimi na temelju raziskav na terenu in bibliografskih virov. Podaja tudi nekatere predpostavke o morebitnih vzrokih, ki so povzročili hitri upad in posledično izginotje te vrste vzdolž obale Slovenije.
Ključne besede: Fucus virsoides, pojavljanje, izginotje, obala Slovenije, severni Jadran
10
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
REFERENCES
Accurti, G. (1858): Cenno sulle alghe di Capodistria. Programma dell'I.R. ginnasio di Capodistria. Trieste, Lloyd Austr., pp. 1-9.
Alberti, G. & C. Battelli (2002): Un naturalista tra i Frati Minori Conventuali del convento di San Francesco a Pirano: Padre Pio Titius (1801-1884). Atti Mus. Civ. Stor. Nat., Trieste, 49, 213-239.
Ardissone, F. (1886): Phycologia mediterranea. Parte II, Oosporee - Zoosporee - Schizosporee. Tipografía Maj e Malmati, Varese, 336 pp.
Arrontes, J., F. Arenas, C. Fernández, J. M. Rico, J. Oliveros, B. Martínez, R. M. Viejo & D. Alvarez (2004): Effect of grazing by limpets on mid-shore species assemblages in northern Spain. Mar. Ecol. Prog. Ser., 277, 117-133.
ARSO (2015): Environment Agency of the Republic of Slovenia - Ministry of the Environment and Spatial Planning (http://www.arso.gov.si/vode/morje/)
Ballesteros, E., X. Torras, S. Pinedo, M. Garcia, L. Mangialajo & M. de Torres (2007). A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Mar. Poll. Bull., 55: 172-180.
Battelli, C. (1999): Giuseppe Accurti (1824-1907) -Esempio di connubio tra insegnamento e ricerca scien-tifica. Annales, Ser. Hist. Nat., Koper, 9, 1(15), 113-118.
Battelli, C. (2002): The macrophytobenthos on the hard upper midlittoral from two stations of Slovenian coast (Northern Adriatic Sea). Hacquetia, 1(2), 193-203.
Battelli, C. & G. Alberti (2003): Antonio Zaratin (1846-1923): Raccoglitore e preparatore d'alghe delTI-stria e del Quarnero. Atti - Cent. Ric. Stor., Rovigno, 33, 643-683.
Battelli, C. (2013): Struktura in dinamika makroben-toških združb alg v mediolitoralu slovenskega morja: doktorska disertacija = Structure and dynamic of midlittoral macrobenthic algal communities of the Slovenian sea: doctoral dissertation. Ljubljana, 146 pp.
Boero, F. & E. Bonsdorff (2007): A conceptual framework for marine biodiversity and ecosystem functioning. Mar. Ecol., 28, 134-145.
Boero, F., J.P. Féral, E. Azzurro, V. Cardin, B. Riedel, M. Despalatovic, I. Munda, P. Moschella, J. Zaouali, S.Fonda Umani, A. Theocharis, K. Wiltshire & F. Briand (2008): Climate warming and related changes in Mediterranean marine biota. CIESM Workshop Monographs, 35, 5-21.
Cervin, G. & P. Áberg (1997): Do littorinids affect the survival of Ascophyllum nodosum germlings? J. Exp. Mar. Biol. Ecol., 218, 35-47.
Chiesa, S. & G.G. Lorenzoni (1980): Erbario e col-lezioni dell'Istituto di Botanica e Fisiologia Vegetale, (p. 18-29). In: AA. VV. - Collezioni Scientifiche dei Mu-sei ed Orto Botanico. Facolta di Scienze MM. FF. NN. dell'Universita degli Studi di Padova, Padova, 64 pp.
De Min, R. & E. Vio (1997): Molluschi conchiferi del litorale sloveno. Ser. Hist. Nat., 11: 241-258.
Dethier, M.N. & D.O. Duggins (1984): An indirect commensalism' between marine herbivores and the importance of competitive hierarchies. Am. Nat., 124, 205-219.
Falace, A., G. Alongi, M. Cormaci, G. Furnari, D. Curiel, E, Cecere & A. Petrocelli (2010): Changes in the benthic algae along the Adriatic Sea in the last three decades. Chem. Ecol. 26(1), 77- 90.
Gessner, F. (1969): Photosynthesis and ion loss in the brown algae Dictyopteris membranacea and Fucus vir-soides. Mar. Biol., 4, 349-351.
Gessner, F. & L. Hammer (1971): Physiologische Untersuchung über die Toleranz von Fucus virsoides (Don.) J.Ag. Int. Rev. ges Hydrobiol., 56, 581-597.
Giaccone, G. & S. Pignatti (1967): Studi sulla produtti-vita primaria del fitobentos nel Golfo di Trieste. - II. La ve-getazione del Golfo di Trieste. Nova thalassia, 3(2), 1-28.
Hawkins, S.J., R.G. Harnoll, J.M. Kain & T.A. Norton (1992): Plantanimal interactions on hard substrata in the north-east Atlantic. In: John DM, Hawkins SJ, Price JH (eds) Plantanimal interactions in the marine benthos. Clarendon Press, Oxford, pp. 1-32.
Jackson, J.B.C., M.X. Kirby, W.H. Berger, K.A. Bjorn-dal, L.W. Botsford, B.J. Bourque, R.H. Bradbury, R. Cooke, J.A. Estes, T.P. Hughes, S. Kidwell, C.B. Lange & R.R. Warner (2001): Historical overfishing and the recent collapse of coastal ecosystems. Science, 293, 629-638.
Jenkins, R.J., S.J. Hawkins & T.A. Norton (1999): Direct and indirect effects of a macroalgal canopy and limpet grazing in structuring a sheltered inter-tidal community. Mar. Ecol. Prog. Ser., 188, 81-92.
Jonsson, P.R., L. Granhag, P.S. Moschella, P. Aberg, S.J. Hawkins & R. Thompson (2006): Interactions between wave action and grazing control the distribution of intertidal macroalgae. Ecology, 87(5), 1169-1178.
Johnson, M.P., M.T. Burrows, R.G. Hartnoll & S.J. Hawkin, (1997): Spatial structure on moderately exposed rocky shores: patch scales and the interactions between limpets and algae. Mar. Ecol. Prog. Ser., 160, 209-215.
Johnson, M.P., M.T. Burrows & S.J. Hawkins (1998):
Individual based simulations of the direct and indirect effects of limpets on a rocky shore Fucus mosaic. Mar. Ecol. Prog. Ser., 169, 179-188.
Kashta, L. (1995-1996): Rreth perhapjes dhe ekolo-gjise se Fucus virsoides J. Agardh ne brigjet e Shqiperise. (About the distribution and ecology of Fucus virsoides J. Agardh along the Albanian coast). - Universiteti i Sh-kodres "Luigj Gurakuqi", Buletini i Shkencave Seria Sh-kencave Natyrore, nr., 48(1), 60-65.
Kremer, B.P. & I.M. Munda, (1982): Ecophysiolo-gical studies of the Adriatic seaweed, Fucus virsoides. Mar. Ecol., 3(1), 75-93.
Linardic, J. (1949): Studije o jadranskom fukusu (Fucus virsoides). Zagreb, Acta Botanica, 12, 13, 7-131.
11
ANNALES ■ Ser. hist. nat. ■ 26 ■ 2016 ■ 1
Claudio BATTELLI: DISAPPEARANCE OF FUCUS VIRSOIDES J. AGARDH FROM THE SLOVENIAN COAST (GULF OF TRIESTE, NORTHERN ADRIATIC), 1-12
Lipej, L., M. Orlando-Bonaca & T. Makovec (2004):
Raziskovanje biodiverzitete v slovenskem morju. Morska biološka postaja, Nacionalni inštitut za biologijo. Piran, 136 pp.
Lipej, L., R. Turk & T. Makovec (2006): Endangered species and habitat types in the Slovenian Sea. Zavod RS za varstvo narave. Ljubljana, 264 pp.
Lipizer, M., G. Bressan, G. Catalano & L.A. Ghirar-delli (1995): Adaptability of Fucus virsoides J.Ag. (Fuca-les, Chromophycophyta) to habitat variations in the Gulf of Trieste, North Adriatic Sea. Oebalia, 21, 51-59.
Mačic, V. (2006): Distribution of seaweed Fucus virsoides J. Agardh in Boka Kotorska Bay (South Adriatic Sea). Annales, Ser. Hist. Nat., Koper, 16, 1-4.
Matjašič, J. & J. Štirn (1975): Flora in favna severnega Jadrana. Ljubljana, Pris. 1., Slovenska Akademija Znanosti in Umetnosti, razprave, 4, 19-23.
Munda, M.I. (1972): Seasonal and ecologically conditioned variations in the Fucus virsoides association from the Istrian coast (Northern Adriatic). Dissertationes Slovenska Akademija Znanosti in Umetnosti, 15, 1-33.
Munda, I.M. & B.P. Kremer (1977): Chemical composition and physiological properties of fucoids under conditions of reduced salinity. Mar. Biol., 41, 4-15.
Munda, I.M. (1981): The effect of heavy metals on the growth and some chemical constituents of the brown alga Fucus virsoides (Don.) J. Agardh. Rapp. Comm. int. Mer Médit., 27, 233-234.
Munda, I.M. (1982): The effect of organic pollution on the distribution of fucoid algae from the Istrian coast (vicinity of Rovinj) Acta Adriat., 21, 333-354.
Munda, M.I. (1991): Algal resources in polluted sites of the Northern Adriatic (vicinity of Piran). Acta Adriati-ca, 32, 2, 683-704.
Munda, I.M. (1993a): Changes and degradation of seaweeds stands in the Northern Adriatic. Hidrobiologia, 260/261, 239-253.
Munda, I.M. (1993b): Impact of pollution on benthic marine algae in the Northern Adriatic. International J. Environ. Stud., 43, 185-199.
Munda, I.M. & M. Veber (1996): Simultaneous effects of trace metals and excess nutrients on the Adriatic seaweed Fucus virsoides (Don.) J. Ag. (Phaeophyceae, Fucales). Bot. Mar., 39, 297-309.
Munda, I.M. (1997): Fucus virsoides (Don.) J. Ag. as indicator of changing environments in the Adriatic Sea. Phycologia, 36, 75.
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 He-dwigia, 71, 1-36.
Munda, I.M. (2008): Benthic marine algae as reflection of environmental changes in the Northern Adriatic Sea - Climate warming and related changes in Mediterranean marine biota - Helgoland, 27-31 May 2008, CIESM Workshop Monogr., 35, 65-72.
Ogorelec, B., J. Faganeli, M. Mišič & B. Čermelj (1997): Reconstruction of paleoenvironment in the bay of Koper (Gulf of Trieste, Northern Adriatic). Annales, Ser. Hist. Nat., Koper, 11, 187-200.
Orlando-Bonaca, M., P.A. Mannoni, D. Poloniato & A. Falace (2013): Assessment of Fucus virsoides distribution in the Gulf of Trieste (Adriatic Sea) and its relation to environmental variables. Bot. Mar., 56(5/6), 451-459.
Pavlovec, R. (1985): Numulitine iz apnencev pri Izoli (SW Slovenija). Razprave 4. razred Slovenska Akademija Znanosti in Umetnosti, 26, 219-230.
Pignatti, S. (1962): Associazioni di alghe marine sulla costa veneziana. Venezia, 1st. Ven. Sci. Lett. Art., 33, 3-131.
Rindi, F. & C. Battelli (2005): Spatio-temporal variability of intertidal algal assemblages of the Slovenian coast (Gulf of Trieste, northern Adriatic Sea). Bot. Mar., 48, 96-105.
Schiffner, V. & A. Vatova (1938): Le alghe della laguna di Venezia in La laguna di Venezia, 3, 250 pp.
Štirn, J. (1965): Onesnaženje (kontaminacija) morja v Tržaškem zalivu. Varstvo narave II-III, 157-184.
Turk, V., P. Mozetič & A. Malej (2007): Overview of eutrophication-related events and other irregular episodes in Slovenian sea (Gulf of Trieste, Adriatic sea). Annales, Ser. Hist. Nat., Koper, 17(2), 197-216.
Underwood, A.J. & P. Jernakoff (1981): Effects of interactions between algae and grazing gastropods on the structure of a low-shore intertidal algal community. Oecologia, 48, 221-233.
Viejo, R.M., P. Aberg, G. Cervin & M. Lindegarth (1999): The interactive effects of adult canopy, germling density and grazing on germling survival of the rock-weed Ascophyllum nodosum. Mar. Ecol. Prog. Ser., 187, 113-120.
Vouk, V. (1938): Bilješke o Jadranskom Fukusu (Fucus virsoides) (Don.) J. Ag.). Godišnjak Oceanografskog instituta, Split, Sv., I, 153-159.
Vukovič, A. (1980): Asociacije morskih bentoških alg v Piranskem zalivu. Biološki vestnik, 28(2), 103-124.
Vukovič, A. (1982): Bentoška vegetacija Koprskega zaliva. Acta Adriat., 23(1/2), 227-235.
12