Environ Monit Assess (2015) 187:86 DOI 10.1007/s10661-014-4250-3
Spatial distribution and multiannual trends of potentially toxic microalgae in shellfish farms along the Sardinian coast (NW Mediterranean Sea) Anna Maria Bazzoni & Tiziana Caddeo & Silvia Pulina & Bachisio M. Padedda & Cecilia T. Satta & Nicola Sechi & Antonella Lugliè Received: 13 June 2014 / Accepted: 29 December 2014 # Springer International Publishing Switzerland 2015
Abstract In this study, the geographical distribution and multiannual trends of potentially toxic harmful algal species (HAS) were analysed at 18 mussel farms in Sardinia (Italy, North-Western Mediterranean Sea) using data derived from the Sardinian Regional Monitoring Programme (1988–2012). The results showed an increasing number of potentially toxic microalgae over the study period. Alexandrium catenella and Alexandrium minutum were the most harmful species detected. From 2002 to 2009, these species caused eight paralytic shellfish poisoning-positive events which temporarily stopped commercial trade of mussels. The statistical analysis indicated that some taxa exhibited temporal increasing trends in their abundance (e.g. Pseudo-nitzschia spp.), significant decrements (e.g. Dinophysis sp.), or both increasing and decreasing significant trends (e.g. A. minutum) at different sites, indicating the necessity of further in-depth studies, especially on certain taxa. Overall, the statistical elaboration of the long-term data provided useful signals for early detection of shellfish contamination by different potentially toxic HAS in defined sites. These signals can be used to develop best management practices.
A. M. Bazzoni (*) : T. Caddeo : S. Pulina : B. M. Padedda : C. T. Satta : N. Sechi : A. Lugliè Department of Architecture, Planning and Design, University of Sassari, Via Piandanna 4, 07100 Sassari, Italy e-mail:
[email protected]
Keywords Harmful algal species . Shellfish farms . Phytoplankton . Multiannual trends . Sardinia
Introduction Italy is the third largest European producer of edible bivalve molluscs, after Spain and France (Istituto di Ricerche Economiche per la Pesca e l′Acquacoltura IREPA 2009). Sardinia is one of the major producers of mussels in Italy; hence, this region has relevant economic and social interests in this commercially important product (Mazzette et al. 2010). The Sardinian mussel farm industry covers a marine surface area of 1262 ha (Table 1) and is managed by 30 companies with over 450 employees. About 11,000 tonnes of bivalves (including Tapes decussatus, Mytilus galloprovincialis, Crassostrea gigas and Ostrea edulis) are produced annually, with an economic value of 20 million Euros (Agenzia regionale per l'attuazione dei programmi in campo agricolo e per lo sviluppo rurale LAORE 2009). The management of mussel farm sites is strictly dependent on the water quality, which is regulated by a continuous monitoring programme (2004/853/EC), started in 1988, that is coordinated by the Prevention Department of Health of the Autonomous Region of Sardinia (Lorenzoni et al. 2013). The regional plan includes an early warning system for the detection of potentially toxic microalgae. After about a decade since the beginning of the monitoring plan, Sannio et al. (1997) reported that potentially toxic algal species were present and abundant in Sardinia bivalve production
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areas. Their appearance in breeding waters can negatively affect human health through the consumption of seafood products. The consumption of bivalves contaminated by algal toxins over defined limits results in intoxication, with the effects ranging from acute to severe, depending on the type and amount of toxins accumulated (Ferrante et al. 2013). Contaminated shellfish have been recorded worldwide in transitional and marine ecosystems. Several studies have documented a global increase in the frequency, magnitude and geographic extent of these events over the last 30 years (Van Dolah 2000; Anderson 2009; Hallegraeff 2010). In Europe, several intoxication outbreaks have been documented since 1961 in a number of countries, including Portugal, the Netherlands, France and Sweden, particularly for diarrhetic shellfish poisoning (DSP) (Reguera et al. 2014). Although no deaths related to DSP have been reported in the literature to date (Ciminiello et al. 2014), human fatalities have occurred as a result of paralytic shellfish poisoning (PSP) (Portugal in 1946 and 1955 attributed to Gymnodinium catenatum) (Vale et al. 2008). In Italy, blooms of potentially toxic harmful algal species (HAS) have occurred both along the Adriatic coast and in the Tyrrhenian Sea. The first DSP episodes were reported in patients who ate mussels originating from the Adriatic Sea (Emilia Romagna region) (Ciminiello et al. 2003). Subsequently, poisoning outbreaks that were associated with blooms of potentially toxic HAS have primarily occurred along the Adriatic coast (in the regions of Marche, Abruzzo, Veneto and Friuli Venezia Giulia) (Pistocchi et al. 2012). Toxic algal blooms (Harmful Algal Blooms, HABs) seriously threaten human health and cause major economic losses to the shellfish industry, because farms must remain closed for several months after outbreaks occur. It remains difficult to predict occurrence of toxic blooms, mainly because of the complexity of the phenomenon. In fact, many biotic and abiotic factors act contemporaneously in determining favourable environmental conditions for potentially toxic HAS affirmations (Moore et al. 2009). Furthermore, HAS which have never occurred in a certain area, may suddenly appear and then rapidly cause problems, even if present at low cellular density. This study aimed (1) to assess the geographic distribution of potentially toxic HAS in the shellfish farming sites of Sardinia and (2) to determine long-term trends in their abundance by using multiannual data (1988–
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2012), derived from the Sardinian Regional Monitoring Programme. The evaluation of both the geographic locations and the multiannual dynamics of potentially toxic HAS allows to focus on those sites and species which have been involved in problematic events. The analyses of their temporal and spatial trends represent a useful support in planning most efficient monitoring activities suitable for an early warning to protect public health and shellfish farming activities against economic losses due to harmful blooms. This approach raises the attention towards those sites and species which have been involved in problematic events in the past and which can be considered useful alert signals.
Materials and methods Study area and sampling Sardinia is the second largest island in the NW Mediterranean Sea (Fig. 1). The coastline of the island extends for 1870 km (about a quarter of the Italian total) and hosts a number of aquaculture sites, including fish and mussel farms, both in marine and transitional waters (Table 1). The Sardinian Regional Monitoring Programme started in 1988, with the specific aim of assessing the presence of potentially toxic algae in shellfish farms. This programme was initially run at just three control sites; however, the number of sites has gradually increased, reaching 18 sites by 2012 (Table 2). Three sites have been sampled consecutively for 15 years (FTR, PES, TVC) and one (TOR) for 18 years, while three other sites (CMN, CST, GOR) have been sampled for 21 years but not continuously. The sites were grouped in four different geographical zones (North-East, NE; Central-East, CE; South; Central-West, CW; CE zone includes only one site, representative of the entire area). According to the classification reported into the European Regulation (EC) N. 854/2004, most of the farms are classified as class B production areas (zones in which bivalves can be harvested after a mild treatment) while only one is classified as class A (zones in which bivalves can be collected directly for human consumption) and four as class C (zones in which the bivalves can be harvested only after a long time treatment) (Table 1). The monitoring programme consisted of fortnightly or monthly water samples for the phytoplankton
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Table 1 List of shellfish farms (study sites) and some of their characteristics Zone Site
Code Area
South Santa Gilla
SGL
CW
NE
CE
28.0
Mean depth 1.2
Typology Class Shellfish products
TW
B
Tapes decussatus, Mytilus galloprovincialis, Crassostrea gigas, Ostrea edulis
Colostrai
COL
7.1
0.6
TW
B
Mytilus galloprovincialis
Feraxi
FER
53.0
1.3
TW
B
Mytilus galloprovincialis, Crassostrea gigas
San Giovanni
SGN
13.2
3.0
TW
A
Tapes decussatus, Mytilus galloprovincialis, Crassostrea giga
Cabras
CAB
30.0
1.7
TW
B
Tapes decussatus, Mytilus galloprovincialis
Corru Mannu
CMN
7.7
1.3
TW
B
Tapes decussatus, Mytilus galloprovincialis, Crassostrea gigas
Corru S'Ittiri
CST
161.0
1.0
TW
C
Veneroidae
Foce Tirso
FTR
32.0
2.0
MW
B
Mytilus galloprovincialis
Gulf of Oristano Pauli Biancu Turri III Peschiera
GOR
32.0 14.0
MW
A
Mytilus galloprovincialis
PBT
12.0
TW
C
Temporarily inactive
PES
500.0
2.0
TW
C
Veneroidae
S'Ena Arrubia
SEA
24.8
0.7
TW
B
Tapes decussatus
0.6
Torrevecchia
TVC
72.0
1.8
TW
C
Veneroidae
Gulf of Olbia
GOL 150.0
4.8
MW
B
Mytilus galloprovincialis
Porto Pozzo
PPZ
36.0
0.8
TW
B
Tapes decussatus
San Teodoro
STD
23.5
0.7
TW
A/B
Tapes decussatus, Crassostrea gigas, Ostrea edulis
Cugnana
CUG
0.2
1.0
MW
B
Temporarily inactive
Tortolì
TOR
80.0
1.5
TW
B
Mytilus galloprovincialis, Crassostrea gigas, Ostrea edulis
Area is reported in hectares (ha) TW transitional waters, MW marine waters, NE North-East, CE Central-East, CW Central-West
qualitative and quantitative analysis. No environmental data were collected. The samples (1 L) were taken directly in clean PE bottles at a depth of 0.5 m from the surface, without particular sampling devices. No water samples were taken on the bottom, due to the shallowness of the majority of the farming sites (Table 1) and the sub-surface position of the mussels. The frequency of samplings increased when mussel toxicity exceeded the legal limits (Ministerial Decree of 16 May 2002). In these cases, an extraordinary sampling plan was adopted, with controls even every 2 days and sometimes with an extension to a greater number of stations. Phytoplankton Samples for phytoplankton analyses were fixed in situ with Lugol’s iodine solution or formaldehyde (4 %) and examined within 24 h using settling chambers under an inverted microscope (Zeiss Axiovert 25). Species abundances in fixed samples were determined with the
Utermöhl’s method (1958). Depending on phytoplankton cell densities, the analysed sub-samples varied from 5 to 100 cm3. All specimens of potentially toxic HAS included in the list provided by the Italian Ministry of Health were counted on the whole surface of the settling chamber at a magnification of×200. Data regarding non-potentially toxic species presence and abundance are available but not included in this study. Since the beginning of potentially toxic HAS monitoring programme, few operators worked at microscope, acting with a unique and reliable method. For species identification, live samples were also observed. For the identification of Alexandrium, the cells were stained with Calcofluor (Fritz and Triemer 1985) and examined under an Axiovert 100 inverted microscope with UV epifluorescence (Axioplan, filter set Zeiss 487902, ×1000 magnification). Morphology and arrangement of thecal plates were reconstructed following Balech (1995). Scanning electron microscope (SEM) was used in few cases. Identification of potentially toxic HAS was based also on Schiller (1933), Cupp (1977), Rampi and
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Fig. 1 Study area and location of shellfish farming sites (circle) in Sardinia
Bernhard (1981), Tomas (1997) and Faust and Gulledge (2002). Statistical analyses The non-parametric Mann–Kendall test (Gilbert 1987) was used to detect significant multiannual trends in potentially toxic HAS abundance at each site. The annual
means of potentially toxic HAS abundances were considered, including only years with 12 months of data and omitting those years in which one or more months were not sampled. The tests were considered significant when the p value was
