Influences of sedimentation and hydrodynamics on the spatial distribution of Alexandrium catenella/tamarense resting cysts in a shellfish farming lagoon impacted by toxic blooms
Highlights
► Alexandrium resting cyst densities were mapped along with sediment structure in the Thau Lagoon (French Mediterranean). ► The highest cyst densities were found in silty sediments, but this link was less strong at stations further away from the Alexandrium bloom area. ► Cyst densities were highly spatially autocorrelated with accumulation sites. ► The hydrodynamics, involved in the dispersal and sedimentation of cysts together with sediment structure, is likely responsible for the cyst distribution pattern.
Introduction
Proliferations of toxic dinoflagellates contribute to phenomena known as harmful algal blooms (HABs), which can lead to accumulations of toxins in seafood organisms, hence generating public health concerns and economic losses due to aquaculture bans (Van Dolah et al., 2001, Hoagland and Scatasta, 2006).
For numerous dinoflagellate species including Alexandrium species, sexual reproduction leads to the formation of resting cysts. Cyst formation increases the survival capacity of the species when exposed to environmental fluctuations exceeding the tolerance range for the survival of vegetative cells. These long-lived, highly resistant cells play a key role in seasonal and inter-annual bloom dynamics through the alternation between this benthic resting stage and the pelagic stage represented by planktonic vegetative cells (for a review, see Genovesi-Giunti et al., 2006). The germination of resting cysts provides the seeding source of blooms when environmental conditions favorable to this process are similar to those favorable to vegetative growth. Consequently, for cyst-forming species, the presence of resting cysts in coastal sediments can be considered a marker for the existence of an established population for a given species. Hence, the identification of cyst-forming harmful algal species in sediments and the location of cyst accumulations could be an appropriate complement to studies of planktonic populations for the detection of potential seeding sources for bloom initiation.
In sediments containing high cyst densities, resting cysts have mostly been found in the first 3 cm of sediment (e.g., Erard-Le Denn et al., 1993, Irwin et al., 2003, Genovesi et al., 2007). Important cyst banks have been reported in enclosed areas such as bays, harbors or lagoons (Itakura and Yamagushi, 2001, Garcés et al., 2004, Pospelova et al., 2004, Anglès et al., 2010, Satta et al., 2010) and have been linked to occurrences of dense vegetative cell blooms (Garcés et al., 2004, Joyce et al., 2005, Olli and Trunov, 2010). Several studies have reported that cyst accumulations were favored in fine or muddy sediments (with a high organic matter content) rather than in sandy substrates in various coastal marine systems (Kremp, 2000, Yamaguchi et al., 1996, Joyce et al., 2005, Gayoso, 2001, Matsuoka et al., 2003, Wang et al., 2004, Anglès et al., 2010). However, the linkage between sediment structure and cyst densities is not yet well understood.
In the Thau Lagoon (French Mediterranean Sea), seasonal Alexandrium blooms have been a recurrent paralytic shellfish poisoning (PSP) threat for the shellfish farming industry since 1998 (Genovesi et al., 2011). The toxic blooms mostly take place in a shallow, thumb-shaped cove named Crique-de-l’Angle in the northern part of the lagoon (Fig. 1), as established by a regular weekly survey by REPHY (IFREMER's French national network for monitoring phytoplankton and phycotoxins). Then, depending on winds and hydrodynamic conditions, toxic planktonic cells can be transported from the bloom area to nearby farmed oysters, which can lead to a paralytic shellfish toxin (PST) contamination alert and can eventually be spread further into the lagoon. For instance, the highest abundance of vegetative cells recorded during the bloom of autumn 2003 in Crique-de-l’Angle was ∼4.5 × 106 cells L−1 and resulted in water discoloration lasting several days (Genovesi et al., 2011). Molecular genetics studies on rDNA revealed that the toxic species Alexandrium catenella, corresponding to the group IV ribotype of the Alexandrium tamarense complex as defined by Lilly et al. (2007), is accompanied by a non-toxic A. tamarense corresponding to the group III ribotype (Genovesi et al., 2011). These two species have morphologically identical resting cysts (Fukuyo, 1985), and for convenience, these will be thereafter designated as A. catenella/tamarense resting cysts.
The present work was aimed at assessing the densities of resting cysts belonging to A. catenella/tamarense across Thau Lagoon sediments. Cyst densities were first analyzed across the whole Thau Lagoon following a large-scale sampling grid (1000 m × 1000 m). Subsequently, a finer scale (100 m × 100 m) sampling grid was used in the area affected by these Alexandrium blooms (the Crique-de-l’Angle Cove). At both scales, several descriptors of sediment quality (5 granulometric fractions < 2 mm, as well as water, organic matter, nitrogen and phosphorus contents) were surveyed to investigate whether the resting cyst distribution could be linked to sediment structure. A statistical analysis using spatial autoregressive models was performed to determine whether the cyst distribution might exhibit an organized spatial structure with favored accumulation sites. These observations regarding cyst abundances with respect to sediment structure were used to infer the role of hydrodynamics in the dispersal and settlement of resting cysts in the Thau Lagoon, and to discuss the potential for these cyst banks to initiate new blooms.
Section snippets
Study area
The Thau Lagoon, located in the south of France along the Mediterranean coast (Fig. 1), is a large and shallow marine water body (75 km2; depth <10 m; mean depth 4.5 m) that is connected to the Mediterranean Sea by two narrow channels. The Thau Lagoon is the most important shellfish farming site on the Mediterranean coast of France.
The lagoon's bathymetry has been described by Dueri et al. (2010). The wind regime is mostly dominated by N/NW alternating with E/SE winds (Souchu et al., 2001). The
Characterization of sediments across stations
The whole dataset, including sediment descriptors and cyst densities, is provided in Supplementary Table 1. In the Thau Lagoon sediments obtained from the large-scale sampling grid, the contents of biochemical components (H2O, OM, TN and TP) were all highly correlated (Pearson's correlation test, Supplementary Table 2). These were also correlated with muddy fractions F < 2 and F2–20 and negatively correlated with sandy fractions F50–200 and F > 200 (Supplementary Table 2). Therefore, TN and TP
Patterns of resting cyst densities
Compared to other areas with Alexandrium spp. blooms, the mean density of A. catenella/tamarense resting cysts in the Thau Lagoon was relatively low (20 cysts g−1 DS in the whole lagoon analysis and 80 cysts g−1 DS in Crique-de-l’Angle). For example, in areas of Australia, Japan and USA impacted by Alexandrium spp. blooms with >106 cells L−1, hundreds to thousands cysts per cm3 of sediment have been reported (Yamaguchi et al., 1996, Hallegraeff et al., 1998, Anderson et al., 2005, Horner et al., 2011
Conclusions
Relatively high and homogeneous cyst densities in Crique-de-l’Angle, where A. tamarense/catenella blooms develop, contrast with the low and heterogeneous cyst densities in the main lagoon, where vegetative cells and resting cysts have to be transported by wind-induced currents generated during periods of strong wind. The cyst densities across the Thau Lagoon were spatially autocorrelated, indicating that some forcing environmental conditions likely influenced the dispersal, settlement and
Acknowledgments
This study has been conducted with support from the Region Languedoc-Roussillon through a Ph.D. fellowship granted to B.G., and with financial support from the Programme National d’Environnement Côtier (PNEC-France). The authors thank P. Cecchi and Y. Collos for their helpful discussions and comments on an early version of the manuscript. The authors also thank IFREMER LER/LR for assistance and logistical support, in particular, J. Oheix, P. Le Gall and F. Lagarde for their assistance in
References (69)
- et al.
Alexandrium fundyense cyst dynamics in the Gulf of Maine
Deep Sea Research II
(2005) - et al.
Alexandrium minutum resting cyst distribution dynamics in a confined site
Deep Sea Research II
(2010) - et al.
Oligotrophication and emergence of picocyanobacteria and a toxic dinoflagellate in Thau lagoon, southern France
Journal of Sea Research
(2009) - et al.
The role of resting cysts in Alexandrium minutum population dynamics
Deep Sea Research II
(2010) - et al.
A preliminary evaluation of wave attenuation by four species of seagrass
Estuarine, Coastal and Shelf Science
(1992) - et al.
Towards an optimal sampling strategy for Alexandrium catenella (Dinophyceae) benthic resting cysts
Harmful Algae
(2007) - et al.
Spatial distribution of benthic cysts of Alexandrium catenella in surface sediments of Puget Sound, Washington, USA
Harmful Algae
(2011) - et al.
Cyst and radionuclide evidence demonstrate historic Gymnodinium catenatum dinoflagellate populations in Manukau and Hokianga Harbours, New Zealand
Harmful Algae
(2003) - et al.
Dinoflagellate cysts from surface sediments of Saldanha Bay South Africa: an indication of the potential risk of harmful algal blooms
Harmful Algae
(2005) - et al.
Seasonal dynamics in mixed eelgrass beds, Zostera marina L. and Z. noltii Hornem. in a Mediterranean coastal lagoon (Thau lagoon, France)
Aquatic Botany
(1999)