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Pseudochattonella verruculosa

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Pseudochattonella verruculosa

Summary

  • Last modified
  • 16 November 2018
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Pseudochattonella verruculosa
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Plantae
  •     Phylum: Heterokontophyta
  •       Class: Dictyochophyceae
  •         Order: Florenciellales
  • Summary of Invasiveness
  • Over recent decades P. verruculosa has not only increased in abundance in coastal waters of Japan, but has been found in tidal estuaries and lagoons on the eastern coast of the United States, and off the coasts o...

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Identity

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Preferred Scientific Name

  • Pseudochattonella verruculosa (Y. Hara et Chihara) Tanabe-Hosoi, Honda, Fukuya, Inagaki & Sako, 2007

Other Scientific Names

  • Chattonella verruculosa Y. Hara et Chihara in Hara, Doi et Chihara, 1994
  • Verrucophora verruculosa (Y. Hara et Chihara) Eikrem 2007

Local Common Names

  • Japan: "burr-shaped" Chattonella

Summary of Invasiveness

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Over recent decades P. verruculosa has not only increased in abundance in coastal waters of Japan, but has been found in tidal estuaries and lagoons on the eastern coast of the United States, and off the coasts of Germany and New Zealand. Its sibling species Pseudochattonella farcimen, although of uncertain geographic origin, has bloomed recurrently in Scandinavian waters since identification in 1998. The species are therefore showing invasive traits in disjunct geographical regions with apparent potential to spread more widely in temperate inshore waters.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Plantae
  •         Phylum: Heterokontophyta
  •             Class: Dictyochophyceae
  •                 Order: Florenciellales
  •                     Genus: Pseudochattonella
  •                         Species: Pseudochattonella verruculosa

Notes on Taxonomy and Nomenclature

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The name Chattonella verruculosa, along with three other Chattonella species, was first published as a nomen nudum in the book “Red tide organisms in Japan” (Fukuyo et al., 1990). The four species were subsequently validly published in Hara et al. (1994). In 2007 Chattonella verruculosa was independently renamed as Pseudochattonella verruculosa by Hosoi-Tanabe et al. (2007) and as Verrucophora verruculosa by Edvardsen et al. (2007). The first of these names, Pseudochattonella verruculosa, has priority.

From 1998, recurrent extensive blooms of an heterokont flagellate similar to Pseudochattonella verruculosa have been reported from the North Sea, the Skagerrak (the strait running between the southern coast of Norway, the southern coast of Sweden and the Jutland Peninsula of Denmark), and the Kattegat (Henriksen, 2009) raising speculation that the organism could have been introduced in ballast water from Japan. Initially considered to be a raphidophyte and referred to as Chattonella aff. verruculosa, molecular sequencing subsequently unambiguously indicated this organism to be a dictyophyte and genetically distinct from P. verruculosa (Edvardsen et al., 2007)
 
The Scandinavian organism was renamed as Verrucophora farcimen Eikrem, Edvardsen et Throndsen (in Edvardsen et al., 2007). However, as Pseudochattonella Hosoi-Tanabe, Honda, Fukaya, Inagaki et Sato (in Hosoi-Tanabe et al., 2007) has priority over Verrucophora Eikrem, Edvardsen et Throndsen, V. farcimen  has since been transferred to the former genus Pseudochattonella by Riisberg (2008).
 
The first published use of the combination Pseudochattonella farcimen was as P. farcimen Eikrem, Edvardsen et Throndsen in Riisberg and Edvardsen (2008), incorrectly citing Edvardsen et al. (2007) as the source. Riisberg and Edvardsen (2008) also incorrectly credit the genus Pseudochattonella to Eikrem, Edvardsen et Throndsen, and the combination P. verruculosa to Eikrem, again citing Edvardsen et al. (2007) as the source paper. The combination was validly published by Eikrem et al. (2009) and the correct nomenclature for this second species of Pseudochattonella is:
 
Pseudochattonella farcimen (Eikrem, Edvardsen et Throndsen) Eikrem in Ekrem, Edvardsen et Throndsen, 2009
Basionym:  Verrucophora farcimen Eikrem, Edvardsen et Throndsen
 
The icthyotoxic algae reported as Chattonella cf. verruculosa from coastal Delaware, USA (Bourdelais et al., 2002) differs to the Pseudochattonella species in not only its green colouration, but also in phylogenetic analyses, and is possibly a raphidophyte (Edvardsen et al., 2007). The new name Chloromorum toxicum Tomas et al. has been proposed for this taxon (Giner et al., 2008).  
 
Edvardsen et al. (2007) erected a new order, the Florenciellales Eikrem, Edvardsen et Throndsen, to accommodate V. farcimen, V. verruculosa and Florenciella parvula Eikrem. This order remains valid, and contains Pseudochattonella farcimen, P. verruculosa and F. parvula.

Description

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Cells 12-45 µm in diameter, nearly globose. Two unequal flagellae emerge from the anterior end of the cell, the longer directed anteriorly and undulating during swimming, the shorter trailing. No osmiophilic particles present in the cytoplasm beneath the cell surface. Several warts of large mucocysts, containing bullet-shaped inclusions in the outer half, distributed randomly around the cell periphery and these eject in response to slight changes in environmental conditions; verrucose protrusions of mucocyst heads visible by light microscopy. Discoid chloroplasts numerous, situated mainly in the ectoplasm; chloroplasts pale-yellow to yellow-brown,  relatively small, 2-3 µm long and 1-2.5 µm wide, each with a single embedded pyrenoid. Pyrenoid matrix invaded by a single tubular intrusion originating in the periplastidal space. Spherical nucleus central in the cell. Comparatively large mitochondria located in the endoplasm; smaller ones in the ectoplasm. Contractile vacuoles and eyespots absent (Hara et al., 1994; Hallegraeff and Hara, 2003; Hosoi-Tanabe et al., 2007).

For further descriptions and illustrations see: 
Fukuyo et al. (1990) pages 342-343
Hara et al. (1994) page 417, figs 26-33
Hallegraeff and Hara (2003) page 7, fig. 18.9
 
Culture collections are present in the:
 
Microbial Culture Collection, National Institute for Environmental Studies (NIES – Collection), Tsukuba, Japan (NIES, 2009)
          Pseudochattonella verruculosa  
                          Strain No: NIES-670 Harima-nada, Japan. Isolator: S Yoshimatsu
                          Strain No: NIES-850 Shodo Island, Japan. Isolator: T Sawaguchi
 
Roscoff Culture Collection, Station Biologique, Roscoff, France (RSS, 2009)
          Pseudochattonella verruculosa
Strain No: RCC-1082 Atlantic Ocean – Langesund, southern Norway, 28.iii.2001. Isolator: B Edvardsen
 
Cawthron Institute, New Zealand (CICCM, 2009)
Pseudochattonella verruculosa
Strain No: CAWDC01 (=CAWR21) Kaikoura, New Zealand. Isolator: L Rhodes
Strain No: CAWDC02 (=CAWR22) Taylor’s Mistake, New Zealand. Isolator: J Adamson

Plant Type

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Vegetatively propagated

Distribution

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Type locality: Harima-nada, Tokushima, Japan.

Western Japan in the Seto Inland Sea and in Hakata Bay in Kyushu (Hara et al., 1994); East coast USA in Chesapeake Bay (Marshall et al., 2005a,b) and South Carolina (Hayes and Lewitus, 2003); New Zealand (Bowers et al.,  2006); Tasmania, Australia (G Hallegraeff, University of Tasmania, personal communication, 2009); Germany (Riisberg and Edvardsen, 2008) and the Netherlands (Riisberg, 2008).
 
Known from coastal waters (Hara et al., 1994), bays and tidal tributaries (Marshall et al., 2005a,b), and brackish lagoons (Hayes and Lewitus, 2003).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Sea Areas

Atlantic, NortheastLocalised2000IntroducedRiisberg and Edvardsen, 2008
Atlantic, NorthwestLocalised2008IntroducedMarshall et al., 2005; Marshall et al., 2005
Atlantic, Western CentralLocalised2003IntroducedHayes and Lewitus, 2003
Pacific, NorthwestPresentNativeHosoi-Tanabe et al., 2007
Pacific, SouthwestPresent2003IntroducedBowers et al., 2006

Asia

JapanPresentNativeHosoi-Tanabe et al., 2007
-KyushuPresentNativeHara et al., 1994

North America

USAPresentPresent based on regional distribution.
-South CarolinaPresentIntroducedHayes and Lewitus, 2003Brackish lagoons
-VirginiaPresentIntroducedMarshall, 2003; Marshall et al., 2005; Chesapeake Bay Program, 2007; Marshall et al., 2009Noted as rare in Chesapeake Bay and also its tidal tributaries

Europe

GermanyLocalised2000IntroducedRiisberg and Edvardsen, 2008
NetherlandsPresent2006IntroducedRiisberg, 2008

Oceania

New ZealandPresentIntroducedBowers et al., 2006; Riisberg and Edvardsen, 2008

History of Introduction and Spread

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In the coastal waters of Japan, the abundance of Pseudochattonella verruculosa appears to have increased over recent decades. P. verruculosa, along with Heterocapsa circularisquama (Dinophyceae), have been said to have caused ‘novel red tides’ in the coastal waters of western Japan because they have only been identified there since the late 1980s (Yamaguchi et al., 1997). Since that time they have replaced red tide species such as Chattonella antiqua, Chattonella marina and Heterosigma akashiwo) and, leading up to 1997, became the predominant causative organism of harmful red tides (Yamaguchi et al., 1997).

On the eastern coast of the USA, extensive phytoplankton monitoring programmes in Chesapeake Bay and Virginia tidal estuaries did not record P. verruculosa prior to 1996; however, it has been found since (Marshall, 2003), and also in brackish lagoons in South Carolina (Hayes and Lewitus, 2003). A bloom of Pseudochattonella in Germany in 2000 was later determined to be P. verruculosa, and the species was also isolated from New Zealand waters in 2003 (Riisberg and Edvardsen, 2008).
 
The first apparent occurrence of Pseudochattonella farcimen in Scandinavian waters is widely reported to have been in 1998 (Karlson, 2007), and it has occurred there every year since, becoming a characteristic dominant spring species (Riisberg and Edvardsen, 2008; Henriksen, 2009). However, “Chattonella” like cells were found to be present in low concentrations since 1993 when older samples from the Swedish coast were re-examined (Naustvoll, 2006). If introduced, the geographic origin of the species remains unknown. However, Riisberg and Edvardsen (2008) consider its presence in other geographic regions cannot yet be discounted, in part because the form variability and fragility of Pseudochattonella cells during fixation could lead to misidentification in environmental samples. A bloom of P. farcimen was observed in the southern part of the Gulf of Gdansk in the spring of 2001 (Lotocka, 2009).
 

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Atlantic, Northeast Pacific, Northwest 2000 Hitchhiker (pathway cause)Riisberg and Edvardsen (2008)
Atlantic, Northwest Pacific, Northwest 1996 Hitchhiker (pathway cause)Marshall et al. (2005)
Atlantic, Western Central Pacific, Northwest 2002 Hitchhiker (pathway cause)Hayes and Lewitus (2003)
Pacific, Southwest Pacific, Northwest 2003 Hitchhiker (pathway cause)Riisberg and Edvardsen (2008)

Risk of Introduction

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The increasing distribution and abundance of Pseudochattonella  species in cool temperate waters over the past decade suggests that this species has been introduced to new regions, and could therefore be introduced elsewhere. Ships’ ballast water has been suggested as a possible vector.  

Habitat

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In the Seto Inland Sea of Japan, P. verruculosa is one of the species found in red tide blooms that occur frequently from spring to autumn (Hara et al., 1994).  In the eastern USA, P. verruculosa has been found in Chesapeake Bay and its tidal tributaries, and in brackish lagoons in South Carolina (Hayes and Lewitus, 2003; Marshall et al., 2005a,b).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Brackish
Lagoons Present, no further details Harmful (pest or invasive)
Marine
Inshore marine Present, no further details Harmful (pest or invasive)

Biology and Ecology

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Genetics

Nuclear 18S and plastid 16S sequence data supported the movement of “Chattonella” verruculosa from the Raphidophycae to the Dictyophyceae (Bowers et al., 2006). Cultures from Japan and New Zealand shared 99% sequence similarity in the 18S region and 100% with respect to the plastid 16S locus (Bowers et al., 2006).  

Plastid and mitochondrial DNA and LSU and SSU rDNA have been found to delineate P. verruculosa and P. farcimen (Riisberg and Edvardsen, 2008). This study also found high levels of ITS rDNA polymorphism in the genus, but P. verruculosa isolates from blooms in Germany, Japan and New Zealand were almost identical in five different genes: LSU and SSU rDNA, rbcL, cox1, psbA.
 
GenBank:
 
P. verruculosa              (Bowers et al., 2006)
Strain: NIES 670 Harima Nada, Seto Island Sea, Japan. Isolator: S. Yoshimatsu, 1987
18S: AY788948       16S: AY864040     
 
P. verruculosa              (Bowers et al., 2006)
Strain: CAWR 21 Kaikoura, New Zealand. Isolator: L. Rhodes, 2003
18S: AY788947       16S: AY864049 
 
P. verruculosa              (Edvardsen et al., 2007)
Strain: NIES 670
SSU: AM075625     LSU: AM040504
 
P. farcimen                    (Edvardsen et al., 2007)
Strain: UIO 110   
SSU: AM075624     LSU: AM040499-AM040503
 
Reproductive Biology
 
Asexual reproduction takes place by binary fission while cells are swimming. Cyst formation and sexual reproduction are unknown (Hara et al., 1994). Naustvoll (2006) reports that preliminary experiments to investigate the life cycle of P. farcimen indicate that the species may form resting stages (cysts) under some conditions.
             
Physiology and Phenology
 
The effects of temperature and salinity on the growth of P. verruculosa in culture were investigated to evaluate the relative importance of these factors in the dynamics of natural populations (Yamaguchi et al., 1997). Experiments over a temperature range of 5-30°C and salinity range of 10-35 psu found that this organism did not grow at 10 psu or at temperatures > 25°C and statistical analysis of results found both temperature, salinity and temperature-salinity interaction to have significant effects on growth rates. The highest growth rate reported by Yamaguchi et al. (1997) was 1.74 cell divisions/day at 15°C and 25 psu.
 
Environmental Requirements
 
Red tides of P. verruculosa have been recorded in Fukuoka Bay at a temperature range of 12.3-12.7°C and salinity range of 32.56-32.8 psu (Yamamoto and Tanaka, 1990) and in Tokuyama Bay at temperatures of 18.8-21.5°C and salinities of 32.0-33.09 psu (Baba et al., 1995).
             
P. farcimen is a colder water species with optimal growth at temperatures between 2 and 10°C and all blooms at water temperatures below ~10°C and is known from water bodies with salinities between 12 and 35 psu (Naustvoll, 2006).  

Climate

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ClimateStatusDescriptionRemark
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers

Water Tolerances

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ParameterMinimum ValueMaximum ValueTypical ValueStatusLife StageNotes
Salinity (part per thousand) 25 Optimum 15-35 tolerated
Water temperature (ºC temperature) 15 Optimum 12-22 tolerated

Notes on Natural Enemies

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A virus infecting, and causing lysis in the harmful bloom causing microalga Heterosigma akashiwo (Raphidophyceae) isolated from coastal waters in Japan was found to not similarly cause lysis in Pseudochattonella verruculosa (Nagasaki and Yamaguchi, 1997).

Means of Movement and Dispersal

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Accidental Introduction

Ballast water has been proposed as a possible vector for the movement and dispersal of Pseudochattonella (Hopkins, 2001); however, as for many microorganisms, there is no definitive proof of introduction of these species (Riisberg, 2008).
 

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Hitchhiker Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Ship ballast water and sediment Yes Hopkins, 2001
Ship bilge water Yes
Water Yes

Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Negative

Economic Impact

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Red tides in the Japan Inland Sea have significant impact on the fishing industry. Species of the genus Chattonella (but encompassing P. verruculosa) are major causative organisms and, in 1987, an estimated 2.4 billion yen was lost by the aquaculture industry in the Inland Sea due to red tides caused by Chattonella antiqua (Murayama-Kayano et al., 1998). Blooms of P. verruculosa have been associated with the mortality of fish, including yellowtail, amberjack, and red and black sea bream, in early summer and winter (Yamamoto and Tanaka, 1990; Baba et al., 1995; Yamaguchi et al., 1997). In Chesapeake Bay the presence of Pseudochattonella has not been associated with annual toxic events (Marshall et al., 2005a).

P. farcimen caused the deaths, on the coast of Norway, of 350 tons of farmed salmon in 1998 and 1100 tons in 2001 (Edvardsen et al., 2007), and deaths of garfish, herring, sandeel and mackerel on the west coast of Denmark (Aure et al., 2001; Bourdelais et al., 2002).
 
The mechanism of icthyotoxicity is still uncertain and no toxins have been isolated or characterized from either Pseudochattonella species (Riisberg and Edvardsen, 2008).

Environmental Impact

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As discussed above, P. verruculosa is known to have caused mortalities in wild fish populations.

Risk and Impact Factors

Top of page Invasiveness
  • Abundant in its native range
  • Fast growing
  • Has high reproductive potential
  • Reproduces asexually
Impact outcomes
  • Damaged ecosystem services
  • Negatively impacts livelihoods
  • Negatively impacts aquaculture/fisheries
  • Threat to/ loss of native species
Impact mechanisms
  • Poisoning
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Similarities to Other Species/Conditions

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The two species of Pseudochattonella share with species of Chattonella the presence of two unequal flagella inserted in a shallow depression near the anterior end of the cell (Hara, 1990; Hara et al., 1994; Hallegraeff and Hara 1995; 2003; Hosoi-Tanabe et al., 2007) and the absence of a contractile vacuole and eyespot (Hara et al., 1994; Hosoi-Tanabe et al., 2007). However, Pseudochattonella species differ to Chattonella species in having: mucocysts with bullet-shaped inclusions and verrucose protrusions; an absence of osmiophilic particles in the peripheral cytoplasm; generally smaller cell size (12-45 µm compared to =30 µm); longitudinal axes of the chloroplasts not oriented to the centre of the cell; and an unclear boundary between the endoplasm and ectoplasm (Hara, 1990; Hara et al., 1994; Hallegraeff and Hara, 1995; 2003; Hosoi-Tanabe et al., 2007).

A key to the seven species then ascribed to Chattonella (C. subsalsa, C. verruculosa, C. globosa, C. ovate, C. minima, C. marina and C. antiqua) was provided by Hara et al. (1994). The Random Amplified Polymorphic DNA (RAPD) technique has been successfully applied to distinguish Chattonella antiqua, C. marina, C. ovate and Pseudochattonella verruculosa (Murayama-Kayana et al., 1998). In chemical composition, both Pseudochattonella species contain occelasterol, a rare sterol that had not previously been detected in algae (Giner et al., 2008).
 
P. verrucolosa and P. farcimen, when observed by light microscopy, are both variable in cell size and form, and do not show clear-cut differences with similar appearance and location of chloroplasts, mucocysts, and the type and insertion of flagella (Edvardsen et al., 2007). The ultrastructure is also similar, but in P. verruculosa  the nucleus is round and not branched, and flagella hairs appear to be bipartite rather than tripartite (Edvardsen et al., 2007). The fatty acids of P. farcimen and P. verruculosa  have been found to be very similar to one another, but significantly different to Chattonella marina and Chloromorum toxicum (Giner et al., 2008).
 
P. verruculosa differs to the related Florenciella parvula in having more chloroplasts (many compared to two), in lacking a flagellar swelling, possessing mucocysts, and being larger (12-45 compared to 5 µm) (Hosoi-Tanabe et al., 2007).

Prevention and Control

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Prevention

If Pseudochattonella species are transported in ships’ ballast water as is suspeceted, measures to manage ballast water such as those implemented under the International Maritime Organization Ballast Water Management Convention (IMO, 2004) would reduce the risk of translocation.
 
Eradication
 
Eradication of planktonic microalgae in open coastal waters is not feasible.
 
Control
 
Movement Control
 
In the event of blooms of this species, measure should be implemented to prevent the uptake and translocation of water from the location of the bloom to other regions.

Gaps in Knowledge/Research Needs

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Knowledge on the origin and distribution of both Pseudochattonella species remains uncertain, as are complete details on their life history and environmental requirements, and the mechanism of ichthyotoxicity.

References

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Akizuki Y; Kitakado I; Sasaki M, 1981. Globular type of flagellates occurring at the early stage of Hornellia blooms. Report of previous conjecture and researches of red tides in 1979. Seto Inland Sea Block.

Aure J; Danielssen DS; Skogen M; Svendsen E; Soiland H; Pettersson L, 2001. Environmental conditions during the Chattonella bloom in the North Sea and Skagerrak in May 1998. In: Harmful Algal Blooms 2000 [ed. by Hallegraeff GM, Bolch CJS, Blackburn SI, Lewis R] Paris, : Intergovernmental Oceanographic Commission of UNESCO, 82-85.

Baba T; Momoyama K; Hiraoka M, 1995. A harmful flagellate plankton increased in Tokuyama Bay. Bulletin of Yamaguchi Prefectural Naikai Fisheries Experimental Station (Japan), 24:121-122.

Bourdelais AJ; Tomas CR; Naar J; Kubanek J; Baden DG, 2002. New fish-killing alga in coastal Delaware produces neurotoxins. Environmental Health Perspectives, 110:465-470.

Bowers HA; Tomas C; Tengs T; Kempton JW; Lewitus AJ; Oldach DW, 2006. Raphidophyceae [Chadefaud ex Silva] systematic and rapid identification: sequence analysis and real-time PCR assays. Journal of Phycology, 42:1333-1348.

Chesapeake Bay Program, 2007. A comprehensive list of Chesapeake Bay Basin species 2007. Report EPA 903R-07-004. Annapolis, : United States Environmental Protection Agency.

CICCM, 2009. Cawthron Institute Culture Collection of Micro-algae (CICCM) - Catalogue of strains: May 2009. Website edition. http://www.cawthron.org.nz/aquatic-biotechnologies/downloads/cat-web-may-2009.pdf

Edvardsen B; Eikrem W; Shalchian-Tabrizi K; Riisberg I; Johnson G; Naustvall L; Throndsen J, 2007. Verrucophora farcimen gen. et sp. nov. (Dictyochophyceae, Heterokonta) - a bloom-forming ichthyotoxic flagellate from the Skagerrak, Norway. Journal of Phycology, 43:1054-1070.

Eikrem W; Edvardsen B; Throndsen J, 2009. Renaming Verrucophora farcimen Eikrem, Edvardsen et Throndsen. Phycological Research, 57:170.

Fukuyo Y; Takano H; Chihara M; Matsuoka M, 1990. Red tide organisms in Japan - An illustrated taxonomic guide. Tokyo, : Uchida Rokakuho.

Giner J-L; Zhao H; Tomas C, 2008. Sterols and fatty acids of three harmful algae previously assigned as Chattonella. Phytochemistry, 69:2167-2171.

Hallegraeff GM; Hara Y, 1995. Taxonomy of harmful marine raphidophytes. In: Manual on Harmful Marine Microalgae [ed. by Hallegraeff GM, Anderson DM, Cembella A] Paris, : UNESCO, 365-371.

Hallegraeff GM; Hara Y, 2003. Taxonomy of harmful marine raphidophytes. Second edition. In: Manual on Harmful Marine Microalgae [ed. by Hallegraeff GM, Anderson DM, Cembella A] Paris, : UNESCO, 511-522.

Hara Y, 1990. Chattonella verruculosa Y. Hara et Chihara. In: Red Tide Organisms in Japan - An Illustrated Taxonomic Guide [ed. by Fukuyo Y, Takano H, Chihara M, Matsuoka K] Tokyo, : Uchida Rokakuho, 342-343.

Hara Y; Doi K; Chihara M, 1994. Four new species of Chattonella (Raphidophyceae, Chromophyta) from Japan. Japanese Journal of Phycology, 42:407-420.

Hayes KC; Lewitus AJ, 2003. Nutrient responses of harmful algal blooms in South Carolina brackish lagoonal systems. Journal of Phycology, 39(S1):22-23.

Henriksen P, 2009. Long-term changes in phytoplankton in the Kattegat, the Belt Sea, the Sound and the western Baltic Sea. Journal of Sea Research, 61:114-123.

Hopkins CCE, 2001. Actual and potential effects of introduced marine organisms in Norwegian waters, including Svalbard. Research report 2001-1. Trondheim, : Directorate for Nature Management.

Hosoi-Tanabe S; Honda D; Fukaya S; Otake I; Inagaki Y; Sako Y, 2007. Proposal of Pseudochattonella verruculosa gen. nov., comb. nov. (Dictyochophyceae) for a former raphidophycean alga Chattonella verruculosa, based on 18S rDNA phylogeny and ultrastructural characteristics. Phycological Research, 55:185-192.

IMO, 2004. International Convention for the Control and Managment of Ships' Ballast Water and Sediments, 2004. London, UK: International Maritime Organization.

Karlson B, 2007. Algal situation in marine waters surrounding Sweden, No 2.

Lotocka M, 2009. The first recorded bloom of Pseudochattonella farcimen (Dictyochophyceae, Heterokonta), (Riisberg I., 2008) in the Gulf of Gdansk. Oceanologia, 51:139-143.

Marshall HG, 2003. Toxic algae in Chesapeake Bay. Virginia Journal of Science, 54(2).

Marshall HG; Burchardt L; Lacouture R, 2005. A review of phytoplankton composition within Chesapeake Bay and its tidal estuaries. Journal of Plankton Research, 27:1083-1102.

Marshall HG; Egerton TA; Burchardt L; Cerbin S; Kokocinski MJ, 2005. Long term monitoring results of harmful algal populations in Chesapeake Bay and its major tributaries in Virginia, USA. Oceanological and Hydrological Studies, 34(Suppl. 3):35-41.

Marshall HG; Lane MF; Nesius KK; Burchardt L, 2009. Assessment and significance of phytoplankton species composition within Chesapeake Bay and Virginia tributaries through long-term monitoring program. Environmental Monitoring and Assessment, 150:143-155.

Murayama-Kayano E; Yoshimatsu S; Kayano T; Nishio T; Ueda H; Nagamune T, 1998. Application of the random amplified polymorphic DNA (RAPD) technique to distinguishing species of the red tide phytoplankton Chattonella (Raphydophyceae). Journal of Fermentation and Bioengineering, 85:343-345.

Nagasaki K; Yamaguchi M, 1997. Isolation of a virus infectious to the harmful bloom causing microalga Heterosigma akashiwo (Raphidophyceae). Aquatic Microbial Ecology, 13:135-140.

Naustvoll L-J, 2006. NOBANIS Invasive Alien Species Fact Sheet on Chattonella aff. Verruculosa. Online Database of the North European and Baltic Network on Invasive Alien Species (NOBANIS). http://www.nobanis.org

NIES, 2009. Microbial Culture Collection at National Institute for Environmental Studies. http://mcc.nies.go.jp/

RCC, 2009. Roscoff Culture Collection, Station Biologique Roscoff - Plankton Group. http://www.sb-roscoff.fr/Phyto/RCC

Riisberg I, 2008. Genetic characterization of the marine ichthyotoxic flagellate Pseudochattonella farcimen (Heterokonta) and phylogenetic relationships among heterokonts. Oslo, Norway: University of Oslo. http://www.duo.uio.no/sok/work.html?WORKID=81197

Riisberg I; Edvardsen B, 2008. Genetic variation in bloom-forming ichthyotoxic Pseudochattonella species (Dictyochophyceae, Heterokonta) using nuclear, mitochondrial and plastid DNA sequence data. European Journal of Phycology, 43:413-422.

Riisberg; I; Orr RJS; Kluge R; Shalchian-Tabrizi K; Bowers HA; Patil V; Edvardsen B; Jakobsen KS, 2009. Seven gene phylogeny of heterokonts. Protist, 160:191-204.

Yamaguchi M; Itakura S; Nagasaki K; Matsuyama Y; Uchida T; Imai I, 1997. Effects of temperature and salinity on the growth of the red tide flagellates Heterocapsa circularisquama (Dinophyceae) and Chattonella verruculosa (Raphidophyceae). Journal of Plankton Research, 19:1167-1174.

Yamamoto C; Tanaka Y, 1990. Two species of harmful red tide plankton increased in Fukuoka Bay. Bulletin of Fukuoka Prefectural Fukuoka Fisheries Experimental Station (Japan), 16:43-44.

Links to Websites

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WebsiteURLComment
GISD/IASPMR: Invasive Alien Species Pathway Management Resource and DAISIE European Invasive Alien Species Gatewayhttps://doi.org/10.5061/dryad.m93f6Data source for updated system data added to species habitat list.

Contributors

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02/08/09 Original text by:

John Lewis, ES Link Services Pty Ltd Queensberry Place, North Melbourne, Vic. 3051, Australia

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