Elsevier

Harmful Algae

Volume 25, May 2013, Pages 15-25
Harmful Algae

Influences of sedimentation and hydrodynamics on the spatial distribution of Alexandrium catenella/tamarense resting cysts in a shellfish farming lagoon impacted by toxic blooms

https://doi.org/10.1016/j.hal.2013.02.002Get rights and content

Abstract

Since resting cysts are a potential seeding source for blooms, the presence of these cysts in sediments is a marker of an established population for a number of harmful algal species. The spatial patterns of cyst density in relation to sediment characteristics and hydrodynamics are still largely misunderstood. This study investigated the spatial distribution of resting cysts belonging to the Alexandrium tamarense species complex (Dinophyceae) in sediments of a Mediterranean coastal lagoon (Thau Lagoon, France). This lagoon, hosting shellfish farming, is regularly impacted by toxic Alexandrium catenella blooms. The average cyst density across the whole lagoon was rather low, <20 cysts g−1 of dry sediment (DS). However, densities varied widely among sampled stations, with the highest density (∼440 cysts g−1 DS) recorded in a shallow cove named Crique-de-l’Angle, which is the only area where dense blooms of A. catenella and A. tamarense have been recorded in the years preceding this survey. An analysis using spatial autoregressive models demonstrated that cyst densities were highly spatially autocorrelated (indicating that close stations tended to have more similar cyst densities) with accumulation sites. With respect to sediment characteristics (5 granulometric fractions <2 mm and biochemical components), the highest densities were found in silty sediments containing high proportions of water and organic matter. Nevertheless, the linkage between cyst density and sediment structure was not always verified; this reflected the influence of hydrodynamics on the sedimentation of cysts and sediment particles, and on the dispersal of cysts away from the bloom area by wind-induced currents, suggesting that hydrodynamics was responsible for the spatially autocorrelated distribution of cyst densities.

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)

  • P. Lazure et al.

    An external–internal mode coupling for a 3D hydrodynamical model for applications at regional scale (MARS)

    Advances in Water Resources

    (2008)
  • M. Plus et al.

    Modelling seasonal dynamics of biomasses and nitrogen contents in a seagrass meadow (Zostera noltii Hornem.): application to the Thau lagoon (French Mediterranean coast)

    Ecological Modelling

    (2003)
  • V. Pospelova et al.

    Environmental factors influencing the spatial distribution of dinoflagellate cyst assemblages in shallow lagoons of southern New England (USA)

    Review of Palaeobotany and Palynology

    (2004)
  • J. Terrados et al.

    Experimental evidence of reduced particle resuspension within a seagrass (Posidonia oceanica L.) meadow

    Journal of Experimental Marine Biology and Ecology

    (2000)
  • M. Verlaque

    Checklist of the macroalgae of Thau Lagoon (Herault, France), a hot spot of marine species introduction in Europe

    Oceanologica Acta

    (2001)
  • B. Waeles et al.

    A 3D morphodynamic process-based modelling of a mixed sand/mud coastal environment: the Seine estuary, France

  • E. Abadie et al.

    Contamination de l‘étang de Thau par Alexandrium tamarense

    Episode de novembre à décembre 1998

    (1999)
  • Addinsoft, 2011. XLSTAT 2011, Data Analysis and Statistics Software for Microsoft Excel. Addinsoft, Paris,...
  • D.M. Anderson et al.

    The effects of darkness and anaerobiosis on dinoflagellate cyst germination

    Limnology and Oceanography

    (1987)
  • B. Dale

    Dinoflagellate resting cysts: benthic plankton

  • W. de Boer

    Seagrass–sediment interactions, positive feedbacks and critical thresholds for occurrence: a review

    Hydrobiologia

    (2007)
  • S. Demers et al.

    Resuspension in the shallow sublittoral zone of a macrotidal estuarine environment: wind influence

    Limnology and Oceanography

    (1987)
  • C.F. Dormann

    Effects of incorporating spatial autocorrelation into the analysis of species distribution data

    Global Ecology and Biogeography

    (2007)
  • S. Dueri et al.

    Implementation of a 3D coupled hydrodynamic and contaminant fate model for PCDD/Fs in Thau Lagoon (France): the importance of atmospheric sources of contamination

    International Journal of Environmental Research and Public Health

    (2010)
  • E. Erard-Le Denn et al.

    Alexandrium minutum: resting cyst distribution in the sediments collected along the Brittany coast, France

  • E. Erard-Le Denn et al.

    Resting cysts of Alexandrium minutum in marine sediments: quantification by three methods

  • A. Fiandrino et al.

    A hydrodynamic model for Mediterranean lagoons (MARS-3D): calibration and estimation of water residence time in the Thau lagoon (France)

  • Fiandrino, A., Verney, R., 2010. Développement d’un modèle hydrosédimentaire sur les masses d’eau de transition....
  • M.S. Fonseca et al.

    A comparison of canopy friction and sediment movement between four species of seagrass with reference to their ecology and restoration

    Marine Ecology Progress Series

    (1986)
  • M.J. Fortin et al.

    Spatial Analysis. A Guide for Ecologists

    (2005)
  • Y. Fukuyo

    Morphology of Protogonyaulax tamarensis (Lebour) Taylor and Protogonyaulax catenella (Whedon and Kofoid) Taylor from Japanese coastal waters

    Bulletin of Marine Science

    (1985)
  • E. Garcés et al.

    Relation between vegetative cells and cyst production during Alexandrium minutum bloom in Arenys de Mar harbour (NW Mediterranean)

    Journal of Plankton Research

    (2004)
  • A.M. Gayoso

    Observation on Alexandrium tamarense (Lebour) Balech and other dinoflagellate population in Golfo Nuevo, Patagonia (Argentina)

    Journal of Plankton Research

    (2001)
  • B. Genovesi et al.

    Dormancy and germination features in resting cysts of Alexandrium tamarense species complex (Dinophyceae) can facilitate bloom formation in a shallow lagoon (Thau, southern France)

    Journal of Plankton Research

    (2009)
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      However, it was similar to that detected in tropical zones (Lirdwitayaprasit, 1998; Azanza et al., 2004; Kawamura, 2004) harboring dinoflagellates which are mostly non-cyst forming (Table 6). Interestingly, these fine sediment particles did not seem to influence GML cyst abundance whereas they are known to favor cyst accumulation in other areas (Marcus, 1989; Anglès et al., 2010; Horner et al., 2011; Genovesi et al., 2013). This is in spite of the high percentage of H2O measured at all the sampled stations and the importance of the muddy areas formed by fine sediment particles in the field, previously revealed by Chakroun (2004) as well as in our personal observations.

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